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Bird species that occupy river edge in continuous forest tend to be less sensitive to forest fragmentation

Bird species that occupy river edge in continuous forest tend to be less sensitive to forest... Revista Brasileira de Ornitologia 27(3): 172–186. ARTICLE September 2019 Bird species that occupy river edge in continuous forest tend to be less sensitive to forest fragmentation 1,3 1 2 Barbara Rocha Arakaki Lindsey , Gabriela Menezes Bochio & Luiz dos Anjos Programa de Pós-Graduação em Ciências Biológicas, Universidade Estadual de Londrina, Londrina, PR, Brazil. Departamento de Biologia Animal e Vegetal, Laboratório de Ornitologia e Bioacústica, Universidade Estadual de Londrina, Londrina, PR, Brazil. Corresponding author: barbara.r.a.lindsey@gmail.com Received on 02 October 2018. Accepted on 21 August 2019. ABSTRACT: Along a distance gradient from a given river, two types of habitat can be recognized: natural river edge and forest interior, each one with its own vegetation characteristics and dynamics. In a continuous area of the Brazilian Atlantic Forest, we investigated (1) if bird communities are different between a riverbank of a small stream and an inland forest habitat; (2) if the species of the river edge habitat are the ones that persist in the most in forest fragments after deforestation of a continuous forest; (3) if the river edge habitat species are those that are less sensitive to forest fragmentation. It is expected that there are differences in the bird communities and the occupancy of some species between the two habitats. We allocated 16 sampling points in each of the habitats and sampled the birds by point counts with a short radius of 30 m. Results suggest that there is a significant difference between the composition of the bird communities of the river edge and forest interior habitats, although the species richness is similar. Six species were more likely to occupy the river edge and 14 species had a greater probability of occupancy in the forest interior. Species associated with the river edge habitat (15 species) tend not to be sensitive to forest fragmentation (12 species). In this study, we demonstrated that river-border species of continuous forest areas form a significant part of the bird communities that persist in small forest fragments, with intense edge effect. This shows that not all forest edge species are the result of the colonization from open areas. Congruently, species that occupy the most distant areas from the river vegetation in a continuous forest are those more sensitive to forest fragmentation. KEY-WORDS: Atlantic Rainforest, bird sensitivity, forest interior, natural edge, probability of occupancy. INTRODUCTION tree species; also, it is common to have the fall of trees and consequently the creation of clearings that allow the The Brazilian Atlantic Forest Biome, a tropical forest strip occupation of bamboo species (Bianchini et al. 2001, that stretches along 3300 km of the Brazilian coast beside Anjos et al. 2007). inland areas in Argentina and Paraguay, has thousands This lowland riparian environment constitutes a of endemic species (more than 650 species of vertebrates transition between the river and the associated upland and 8000 species of plants) and is considered one of forest, marking a natural border or ecotone boundary. A the key biodiversity hotspots in the world (Tabarelli et forest ecotone is a consequence of the meeting of distinct al. 2010, Mittermeier et al. 2011). The seasonal-semi- natural plant communities, which, in turn, influences the deciduous forest (SF), a type of forest in the Atlantic diversity of wild animals across the landscape, dependent Forest Biome, extends through the center-south of the on distance from a rivers' edge and the characteristic country interior, between 200 and 800 m of altitude and transition in topography, plant community, hydrological could be considered an ecoregion; there, approximately regimes, and soil types (Naiman et al. 1993, Shirley 2005). 220 tree species occur, 10% of which are endemic to this Considering several taxonomic groups, some studies forest type (Morellato & Haddad 2000, Oliveira-Filho & suggest greater species richness in riparian environments Fontes 2000, Scheer & Blum 2011, Anjos et al. 2018). compared to distinct forest (Naiman et al. 1993), others Locally in SF, many rivers, large and small, and streams found greater richness in non-riparian environments flow from upland areas to the lowland areas, as is common (McGaragal & McComb 1992, Peres 1997) and some along the Atlantic Forest. A distinct riparian environment found no difference between these two habitat types with a unique vegetative formation characterizes those (Gomez & Anthony 1998, Rykken et al. 2007). lowland river edges, which is the focus of the present On birds, several studies indicated the great study. This low land river edges forests usually has a importance of the riparian environment (natural river much less dense canopy with few emerging trees while edges) as a uniquely sustaining habitat with relatively more the under and midstory have a higher density of smaller species than associated upland forest areas (Woinarski Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. et al. 2000, Kajtoch et al. 2007, Dominguez-López & determined for the bird species of SF (see Anjos 2006, Anjos et al. 2011). The hypothesis is that the natural river Ortega-Álvarez 2014, Rannestad et al. 2015, Berduc et edge habitat species are the ones that persist in most of al. 2015, Sekercioglu et al. 2015, Gomez et al. 2016). In a tropical rainforest in Hong Kong, a higher number forest fragments in relation to the forest interior, after of individuals and bird species were recorded in the the deforestation of a continuous forest, that is, those riparian environment, when compared to an area 100– species are less sensitive to forest fragmentation. The reason for this hypothesis is that the vegetation of river 250 m distant from the river due to the high availability edges presents low trees and bushy entanglement in the of adult aquatic insects, which confirms the response of birds to river proximity (Chan et al. 2008). In a 656 lower stratum, phyto-physiognomy that resembles edges ha fragment of the Atlantic Forest in northern Paraná of forest fragments. state, with little topographic variation (~150 m altitude), Anjos et al. (2007) showed that 43% of all bird species METHODS were associated with riparian forest due to differences in vegetation; they sampled 81 species and found that 19 and 45 species were unique to the non-riparian and Study area riparian habitat, respectively. Another study conducted in The study was developed in the Iguaçu National the same site showed that the difference between the bird Park (INP), in the municipality of Céu Azul, Paraná communities is mainly due to the presence of bamboo in o o the riparian forest (Chusquea sp., Willrich et al. 2016). (25 09'12''S; 53 50'42''W, Fig. 1). INP was created in Therefore, riparian bir d species may comprise a significant 1939 and its total area is 185,262.2 ha; it is a fully protected proportion of the overall local forest bird richness and Conservation Unit whose predominant vegetation is SF (ICMBio 2014). In reality, INP is home to the country›s with particular traits associated to that vegetation closer largest continuous SF area. The INP climate, according to rivers. Riparian forest could be in some extension to the classification of Köppen, is of type Cfa subtropical comparable to edges of forest fragments, since both are humid or mesothermic with hot summer, with average ecotones. We argue that edge birds of riparian forest temperatures between 15 and 25 C and rainfall above 900 mm, also distributed throughout the year (Melo et should be more adapted to the edge of forest fragments, al. 2006). while birds inhabiting the interior of the forest avoid those created habitats after deforestation (Gimenes & Anjos SF is related, in virtually the whole area of occurrence, 2003, Hansbauer et al. 2008). In this study, we tested if to a climate of two well defined seasons - one rainy and it is possible that birds that originally live in the riparian one dry (Veloso et al. 1991). The vegetation is dense and presents a great variety of vegetal species, constituted by environment in the continuous forest could be more arboreal elements (perennial or deciduous), as well as tolerant to edges that appear after forest fragmentation. To do this, the first objective of this study was to verify shrub, lianas and epiphytes. Among tree species that are if bird communities are different between a natural river associated with SF are: Assai Palm (Euterpe edulis Mart.), edge habitat and a forest interior. For this, we investigated Peroba (Aspidosperma polyneuron Müll.Arg.), Brazilian Rosewood (Aniba rosaeodora Ducke), Alecrin (Holocalyx the richness and composition of the bird communities. balansae Micheli), Angico-cedro (Parapiptadenia rigida The hypothesis is that the richness and composition of the bird communities of the two habitats are different (Benth.) Brenan) and Argentine Cedar (Cedrela fissilis due to the difference of resour ces found in both habitats, Vell., Guimarães et al. 2003). e.g., the availability of adult aquatic insects in the river Sampling areas natural edge habitat and several resources (both animal and vegetal), associated to the river edge vegetation. The second o bjective of this study was to compare the We sampled two habitats and denominated them as occupancy of the bird species between the two habitats. “River Edge” and “Forest Interior”. The “River E dge” o o In this case, we evaluated the occupancy probability of the (RE; 25 09'43''S; 53 49'39''W) is located on the border of a tributary of the Azul River, and the “Forest Interior” bird species according to the different habitat types. The o o (FI; 25 09'28''S; 53 50'09''W) is located at 300 m of RE, occupancy of some bird species is expected to be different between the two types of habitat, due to differences in at higher altitude (565 m a.s.l.) and at 470 m of forest vegetation. The thir d objective of this study was to verify edge (Fig. 2 in Appendix I). The tributary of the Azul if the river natural edge habitat species are less sensitive to River is a small one, with 8 to 15 m width in the section studied. In each habitat, 16 points were established (Fig. forest fragmentation. In order to do this, we investigated 1). The shortest distance between RE and FI sampling the association between the number of bird species closely related with the river natural edge habitat and their points was 80 m. sensitivity to forest fragmentation, which was previously In RE, points were allocated in four tracks (REA, Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Figure 1. Location of Paraná state in South America and the region of the study in the Iguaçu National Park (INP), western Paraná, southern Brazil. The black dots indicate the location of the sample units (REA, REB, REC and RED in RE and FIA, FIB, FIC and FID in FI). the best-preserved parts, trunk with diameters at breast height (DBH) of more than 1 m (ICMBio 1999). Bird sampling We used the point count method with radius of 30 m (Bibby et al. 1993) in bird sampling. This method is very effective in studies of avian habitat relationships (Anjos et al. 2010). Sampling was carried out during the breeding season of January and February of 2013, in which birds are more likely to be detected by the observer through their vocalizations. Each set of four points in both habitats was Figure 2. Non-metric multidimensional scaling (NMDS) of considered as a sample unit, which was sampled in one bird communities in eight different sample units (REA, REB, day. These sample units were named REA, REB, REC REC, RED, FIA, FIB, FIC, and FID) occurring in two habitats and RED in RE and FIA, FIB, FIC and FID in FI. On (“River Edge” and “Forest Interior”) at INP. each day the points of each sample unit were sampled consecutively 1, 2, 3 and 4, and then again reversing REB, REC and RED), perpendicular to the river. The the sequence, 4, 3, 2 and 1. For example, on track A trails in this habitat were at least 300 m apart (Fig. 2 In in RE, on one day the sampling sequence of the points Appendix I). In FI, the points were allocated on a trail of was REA1, REA2, REA3, REA4, REA4, REA3, REA2, 1200 m located inside the forest. The 16 points located in REA1. The following day the sampling sequence of the this track were subdivided into four blocks of four points points was reversed: REA4, REA3, REA2, REA1, REA1, (blocks FIA, FIB, FIC, FID, Fig. 3 in Appendix I). REA2, REA3, REA4. We sampled each sampling unit for In RE habitat we observe lower trees, with a height two days, and we sampled each sampling point four times of 8 to 15 m, having less plant species richness. Also, the (as if they had been sampled on four mornings). Studies species are adapted to periodic flooding which supports performed in the Atlantic Forest using the point count high humidity (ICMBio 1999). In the transition from RE method demonstrated that 3 to 5 days of sampling are habitat to IF habitat, vegetation changes and trees become sufficient to detect more than 90% of the species recor ded taller. In the FI habitat there is a greater richness of plant in a sample area (Anjos 2007, Cavarzere et al. 2013). species; there are large trees, with maximum heights of Sampling began shortly after sunrise, when daytime 35 m in the emerging layer, and it is common to find in birds start to vocalize, and ended 2.5 h after sampling at Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. the first point, under favorable climatic conditions. We is the probability of the species being present in one place, sampled each point for 10 min with a 10 min interval and the probability of detection (p). between points. According to Anjos et al. (2010), if the Single season occupancy modeling requires multiple observer is interested in assessing differences between visits to sampling units during a season in which species numbers of bird species at different locations, the time can be detected. This model assumes that during these of 10 min is sufficient and in SF, 96% of the species are visits no individual enters or leaves the population (closed recorded during this time interval. model). At each visit the observer detects the presence (“1”) or absence (“0”) of the species of interest. The Statistical analysis absence may be a real absence of the species or a failure to detect the species. This type of modeling adjusts the We estimated the total richness of the bird species using variation in probability of detection while estimating the the non-parametric Chao species estimator (Herzog probability of occupancy of bird species. By incorporating et al. 2002). We evaluated the influence of space the probability of detection into the models, the imperfect (spatial autocorrelation) on the composition of bird detection is considered and the bias in the parameter species through the Mantel test (1000 permutations). estimation is reduced (MacKenzie et al. 2006). The geographic distance matrix was obtained by the Since each point was sampled four times, in each Euclidean distance on the geographical coordinates of sampling we recorded if each species of bird was detected the sample units. We obtained the similarity matrix of or not. Thus, the detection history for each bird species the species composition using the distance of Bray Curtis in each area was obtained. The detection history was on the abundance of the species in each sample unit. We then used to estimate the probability of occupancy of the performed the analysis in R software (R Development species. Core Team 2015), using the package “vegan” (Legendre For this model, the estimated parameters (occupancy & Legendre 1998, Oksanen et al. 2016). and detectability) may be a function of covariates. The We estimated the relative abundance for a single PRESENCE software (Hines 2006) recognizes two species in a habitat (RE or FI), called the Index of Point types of covariates, (1) site-specific covariates, which are Abundance (IPA), by dividing its contact number by constant for the site within the same season, e.g., habitat the total number of points sampled in each site (Bibby type, fragment size, or generalized weather patterns, et al. 1993). To avoid double counting for the same such as drought or El Niño; and (2) sampling-occasion individuals' precautions were taken particularly for those covariates, which may vary at each sampling, such as highly mobile species by adopting a field form that is temperature, precipitation, time of day or observer divided into different quadrants as suggested by Vielliard (Hines 2006). In order to verify the probability of & Silva (1990). Thus, a number of contacts of 30 for occupation of the bird species in each of the habitats, a given species resulted in an IPA equal to 0.468 (30 in the present study the first type of covariant was used. contacts divided by 64 points sampled). Thus, we tested w hether the probability of occupancy of To verify differences in bir d species composition each species of bird occurred as a function of habitat. We between the two habitats we used a permutational analysis ran occupancy models which assumed that the occupancy of variance (PERMANOVA) (Anderson 2001). This and detection of the species were constant - null models analysis was performed in R software (R Development (e.g., same probability of occurrence among all points Core Team 2015), using the packages “vegan” (Oksanen sampled), models that assumed that the probability et al. 2016) and “BiodiversityR” (Kindt & Coe 2005). of species occupancy was in function of the covariant We used non-metric multidimensional scaling habitat, models that assumed that species detection was (NMDS) to visualize the similarity in community a function of covariant habitat and models who assumed composition between the two habitats (Clarke 1993). that the probability of species occupancy and species Data was transformed through weighting dispersion to detection was in function of the covariant habitat. reduce the contribution of high abundance species in We used the Akaike Information Criterion (AIC, the similarity. Similarities of Bray-Curtis were used to Burnham & Anderson 2002) for small sample sizes construct the distance matrices between sample units. (AICc), to select the most parsimonious model. The best This analysis was performed using software PRIMER v. 6 models were those with lower AICc values and higher (Clarke & Gorley 2006). AICc weights; the closer to 1 the AICc weight value, the For each bird species recorded in both habitats, we greater the likelihood of the model being chosen as the calculated the probability of occupancy in the different best (Burnham & Anderson 2002). This analysis was habitats using single-season occupancy modeling performed using PRESENCE 9.0 software (Hines 2006). (MacKenzie et al. 2002). These models involve t he We used a contingency table to investigate the estimation of two parameters: the occupancy (Y), which relationship between the number of birds associated Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. with RE and IF habitats with their sensitivity to forest campanisona, Dendrocolaptes platyrostris, Leptopogon fragmentation (sensitive and non-sensitive). The bir d amaurocephalus, Schiffornis virescens, Cyanocorax chrysops, species' level of sensitivity used was presented in Anjos Trichothraupis melanops, Basileuterus culicivorus). (2006) and Anjos et al. (2011). Anjos (2006) determined Considering the set of species analyzed, 15 bird the sensitivity of the birds to forest fragmentation in SF species were more associated to RE habitat, of which based on samplings carried out in 14 forest fragments three are sensitive and 12 are not sensitive to forest of different sizes and degrees of isolation. Species were fragmentation. Twenty-three bird species were more considered sensitive if they occurred only in control associated to FI habitat, of which 14 are sensitive and 9 fragments or in large, non-isolated fragments; species are not sensitive to forest fragmentation (Appendix IV). not sensitive to forest fragmentation were those that Thus, the data suggest that species of birds susceptible to occurred in all fragments, including the smallest and habitat fragmentation were those associated with the FI most isolated ones (Anjos 2006). In the present study we habitat while those that are not sensitive to fragmentation used two criteria to determine if a given species of bird were those associated with RE habitat ( = 6.13; P = was associated with one of the habitats, RE or FI: 1) the 0.013). species should be exclusive to one habitat and with at least three contacts during the total sampling period; or 2) the species should have a higher probability of occupancy in DISCUSSION one of the habitats. The software Past 3.0 was used to calculate the contingency table (Hammer et al. 2001). We found a significant difference between the The taxonomy and nomenclature followe d American composition of the bird communities of RE and FI Ornithologists' Union - South American Classification habitats, although the species richness was similar. The Committee Checklist for South American Birds (SACC; difference in the composition was due to several exclusive Remsen-Jr. et al. 2016). species in each habitat and to several species that occurred in both habitats but which showed greater occupancy in only one habitat. Species associated with the RE habitat RESULTS tend not to be sensitive to forest fragmentation. In the study by Anjos (2006) on the sensitivity of birds to forest We recorded a total of 80 species of birds in both fragmentation, species that present tolerance to edges habitats, similar to the estimated richness (Chao , 84 ± showed low sensitivity to fragmentation. The results 4 species). We detected no autocorrelation between the of the present study indicate that of the total species geographical distances of the sample units and the species associated to the RE habitat, only 20% are sensitive to composition (Mantel r = 0.063, P = 0.320). We recorded forest fragmentation, while 61% of the species associated 65 bird species in RE and 68 in FI. The number of species to the FI habitat are sensitive to forest fragmentation estimated by Chao for RE was 70 ± 4 species and the (Appendix IV). estimated number for FI was 79 ± 6 species. Therefore, A large number of physical and biological processes we found no difference between the estimated richness of occur from the edge of a fragment because of the influence the two habitats. Twelve species were recorded only in RE of the matrix habitat (Laurance et al. 2011). This influence and 15 were exclusive to FI (Appendix II). on physical and biological processes occurs up to 200– The composition of bird communities differed 500 m from the border into the fragment (Laurance et al. between habitats (PERMANOVA, Pseudo-F = 6.785, P 2011). Therefore, small and/or very elongated fragments < 0.010). In concordance with this result, the ordering are “all edge”, that is, without an interior free of edge of the NMDS showed that the RE and FI sample units effects. These processes can affect forest bir d species. differ in composition and a bundance of bird species, as Species associated with FI, such as Micrastur semitorquatus, they were grouped separately (Fig. 2). Automolus leucophtalmus, Grallaria varia and Schiffornis Among the 53 species that occurred both in RE virescens do not occur in fragments smaller than 60 ha; and FI, the habitat type influenced t he probability of on the other hand, of the 15 species associated with RE, occupancy of 20 species (Appendix III). Six species had about 67% persist in small forest fragments of 11 and a higher probability of occupancy in RE (Melanerpes 25 ha (Anjos 2001). We should highlight that non-forest flavifrons, Xiphocolaptes albicollis, Capsiempis flaveola, colonizer bird species occur in the edge of forest fragments. Platyrinchus mystaceus, Sirystes sibilator, Saltator similis) Those are species from open and/or Cerrado areas, such as and 14 species showed a higher probability of occupation Rupornis magnirostris, Colaptes melanochloros, Melanerpes in FI (Crypturellus obsoletus, Trogon rufus, Pteroglossus candidus, Patagioenas maculosa and Myiarchus swainsoni castanotis, Hypoedaleus guttatus, Dysithamnus mentalis, (Anjos 2001, Baptista et al. 2016, Bierregaard et al. 2016, Conopophaga lineata, Grallaria varia, Chamaeza Joseph 2016, Winkler et al. 2016). Thus, the composition Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. of birds of the edge of a forest fragment should originate by invertebrates (Wilman et al. 2014). Populations at mainly from those living on river banks in continuous the edge of their geographical distribution are generally forest combined with those colonizers from open areas. smaller than those closest to the center of the geographical However, some species of interior forest can also persist in distribution (Holt et al. 2005). The INP is situated on the fragments. Anjos (2001) studied the bird community the southern edge of the geographical distribution of T. in small forest fragments (56, 25 and 11 ha in size). Based coronatus. It is possible that the population of T. coronatus on the present study and in Anjos et al. (2007), we found in the INP is smaller than the population of the species that the majority of the bird species that live in these at the site studied by Cândido-Jr. (2000). Perhaps in small fragments are species that inhabit river bank and/or INP the individuals of this species were concentrated in are colonizing species: 80% in FA, 82% in FB and 84% the habitat RE due to greater availability of some type in FC. of resource or even by competition and the presence of Fragmentation and habitat degradation cause predators. changes in the forest edge, such as increased temperature In this study we demonstrated that river-edge bird and light intensity. In Neotropical forests, birds that live species of a continuous area of forest form a significant on riverbanks in a continuous forest and occupy the edge part of the bird communities that persist in small forest of the remaining habitat after fragmentation and birds fragments, with intense edge effect. This shows that not from open areas should select similar abiotic conditions all the forest edge species are the result of colonization such as air temperature, spatial variation of solar from open habitats. As expected, species that occupy the radiation, humidity and wind speed. On the other hand, most remote areas of the river vegetation in a continuous forest species, such as understory insectivorous birds, forest are those most sensitive to forest fragmentation. select microhabitats with different abiotic characteristics and do not occupy the edge of the small forest fragments or fragments considered “all border” (Pollock et al. 2015, ACKNOWLEDGEMENTS Stratford & Stouffer 2015). In fact, birds associated with darker microhabitats are more sensitive to forest edge This study was funded in part b y the Coordenação de than birds that use brighter microhabitats (Patten & Aperfeiçoamento de Pessoal de Nível Superior - Brasil Smith-Patten 2012). However, the forest interior is also (CAPES) - B.R.A.L. received CAPES “sandwich doctorate” home to several sensitive species to forest fragmentation, scholarship (99999.012747/2013-00) and G.M.B. which are not particularly associated to forest understory, received CAPES “sandwich doctorate” scholarships such as Pionopsitta pileata, one of the most threatened (99999.012746/2013-04). L.d.A. received financial species of psittacines due to the massive destruction of support from CNPq (Brazilian Council for Development their habitat (Sigrist 2013), which occurred exclusively of Science and Technology, Brasilia; 306293/2014-5). in the FI habitat. It is important to point out that in RE Chico Mendes Institute for Conservation of Biodiversity there were also species that were exclusive of that habitat (ICMBio, Brasilia) gave us permission (36241-2) to study and are sensitive to forest fragmentation, such as Coccyzus birds in the Iguaçu National Park, where we had the melacoryphus, Hylopezus nattereri and Tityra cayana. The assistance of PIC Ceu Azul staff. We t hank J.M. Lindsey, reason of these species' sensitivity may be related to the a native speaker from the United States, for English vegetation structure, or even the lower humidity of the proofreading. K. Sieving provided helpful comments and edges of a fragment compared to the river's edge (Pollock suggestions for this manuscript. et al. 2015). 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Sites sampled in the INP: A) “River Edge”, on the edge of a tributary of the Azul River, and B) “Forest Interior”. Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Figure 2. The four points of each of the trails (REA, REB, REC and RED) in the River E dge habitat sampled at INP. Figure 3. The four blocks (FIA, FIB, FIC and FID) of four points located on the trail of FI habitat at INP. APPENDIX II Families and bird species sampled in RE and FI habitats at INP. Taxonomy follows American Ornithologists' Union - South American Classification Committee Checklist for South American Bir ds (Remsen-Jr. et al. 2016). Presence Bird species RE FI TINAMIDAE Crypturellus obsoletus XX Crypturellus parvirostris X Crypturellus tataupa XX COLUMBIDAE Patagioenas picazuro XX Geotrygon montana X Leptotila verreauxi X CUCULIDAE Piaya cayana XX Coccyzus melacoryphus X TROCHILIDAE Phaethornis pretrei X Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Presence Bird species RE FI TROGONIDAE Trogon surrucura XX Trogon rufus XX MOMOTIDAE Baryphthengus ruficapillus XX RAMPHASTIDAE Ramphastos dicolorus XX Selenidera maculirostris XX Pteroglossus castanotis XX PICIDAE Picumnus temminckii X Melanerpes flavifrons XX Colaptes melanochloros X Dryocopus lineatus XX Campephilus robustus XX FALCONIDAE Micrastur semitorquatus X Milvago chimachima X PSITTACIDAE Pionopsitta pileata X Pionus maximiliani XX Pyrrhura frontalis XX Psittacara leucophthalmus XX THAMNOPHILIDAE Hypoedaleus guttatus XX Mackenziaena severa XX Thamnophilus caerulescens XX Dysithamnus mentalis XX Herpsilochmus rufimarginatus XX Drymophila rubricollis X Drymophila malura XX Pyriglena leucoptera XX CONOPOPHAGIDAE Conopophaga lineata XX GRALLARIIDAE Grallaria varia XX Hylopezus nattereri X RHINOCRYPTIDAE Eleoscytalopus indigoticus XX FORMICARIIDAE Chamaeza campanisona XX Chamaeza meruloides XX Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Presence Bird species RE FI FURNARIIDAE Sittasomus griseicapillus XX Dendrocincla fuliginosa XX Dendrocolaptes platyrostris XX Xiphocolaptes albicollis XX Xiphorhynchus fuscus X Lochmias nematura X Anabacerthia lichtensteini XX Automolus leucophthalmus X Synallaxis ruficapilla XX TYRANNIDAE Myiopagis caniceps XX Camptostoma obsoletum XX Capsiempis flaveola XX Leptopogon amaurocephalus XX Hemitriccus diops X Poecilotriccus plumbeiceps XX Tolmomyias sulphurescens X Platyrinchus mystaceus XX Lathrotriccus euleri XX Pitangus sulphuratus X Myiodynastes maculatus X Megarynchus pitangua XX Sirystes sibilator XX TITYRIDAE Tityra cayana X Schiffornis virescens XX INCERTAE SEDIS Piprites chloris X CORVIDAE Cyanocorax chrysops XX TURDIDAE Turdus leucomelas XX THRAUPIDAE Cissopis leverianus X Trichothraupis melanops XX Tachyphonus coronatus X Dacnis cayana X Hemithraupis guira X Conirostrum speciosum XX INCERTAE SEDIS Saltator similis XX Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Presence Bird species RE FI CARDINALIDAE Habia rubica X PARULIDAE Setophaga pitiayumi XX Myiothlypis leucoblephara XX Basileuterus culicivorus XX ICTERIDAE Cacicus haemorrhous XX Cacicus haemorrhous XX FRINGILLIDAE Euphonia pectoralis X APPENDIX III Best models tested for occupancy probability as a function of the different habitat types (RE and FI) at INP, for the bird species that occurred in both habitats. Occupancy (); Probability of detection (p); Difference between the AICc models (ΔAICc). Taxonomy follows American Ornithologists' Union - South American Classification Committee Checklist for South American Birds (Remsen-Jr. et al. 2016). Bird species Model ΔAICc AICc Weight TINAMIDAE Crypturellus obsoletus (habitat),p(.) 0.00 0.40 Crypturellus tataupa (.),p(habitat) 0.00 0.357 COLUMBIDAE Patagioenas picazuro (.),p(.) 0.00 0.386 CUCULIDAE Piaya cayana (.),p(.) 0.00 0.362 TROGONIDAE Trogon surrucura (.),p(habitat) 0.00 0.317 Trogon rufus (habitat),p(.) 0.00 0.448 MOMOTIDAE Baryphthengus ruficapillus (.),p(habitat) 0.00 0.404 RAMPHASTIDAE Ramphastos dicolorus (.),p(.) 0.00 0.459 Selenidera maculirostris (.),p(.) 0.00 0.389 Pteroglossus castanotis (habitat),p(.) 0.00 0.523 PICIDAE Melanerpes flavifrons (habitat),p(.) 0.00 0.369 Dryocopus lineatus (.),p(.) 0.00 0.402 Campephilus robustus (.),p(.) 0.00 0.358 (.),p(habitat) 1.34 0.183 (habitat),p(habitat) 2.57 0.099 Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Bird species Model ΔAICc AICc Weight PSITTACIDAE Pionus maximiliani (.),p(.) 0.00 0.518 (.),p(habitat) 2.48 0.187 (habitat),p(habitat) 4.59 0.034 Pyrrhura frontalis (.),p(.) 0.00 0.323 Psittacara leucophthalmus (.),p(.) 0.00 0.298 THAMNOPHILIDAE Hypoedaleus guttatus (habitat),p(.) 0.00 0.486 Mackenziaena severa (.),p(.) 0.00 0.417 Thamnophilus caerulescens (.),p(.) 0.00 0.358 Dysithamnus mentalis (habitat),p(.) 0.00 0.617 Herpsilochmus rufimarginatus (.),p(.) 0.00 0.502 Drymophila malura (.),p(.) 0.00 0.293 Pyriglena leucoptera (.),p(.) 0.00 0.284 CONOPOPHAGIDAE Conopophaga lineata (habitat),p(.) 0.00 0.482 GRALLARIIDAE Grallaria varia (habitat),p(.) 0.00 0.439 RHINOCRYPTIDAE Eleoscytalopus indigoticus (.),p(habitat) 0.00 0.270 FORMICARIIDAE Chamaeza campanisona (habitat),p(.) 0.00 0.593 Chamaeza meruloides (.),p(.) 0.00 0.3586 FURNARIIDAE Sittasomus griseicapillus (.),p(habitat) 0.00 0.486 Dendrocincla fuliginosa (.),p(.) 0.00 0.376 Dendrocolaptes platyrostris (habitat),p(.) 0.00 0.461 Xiphocolaptes albicollis (habitat),p(.) 0.00 0.360 Anabacerthia lichtensteini (.),p(.) 0.00 0.441 Synallaxis ruficapilla (.),p(.) 0.00 0.485 TYRANNIDAE Myiopagis caniceps (.),p(.) 0.00 0.450 Camptostoma obsoletum (.),p(.) 0.00 0.407 Capsiempis flaveola (habitat),p(.) 0.00 0.468 Leptopogon amaurocephalus (habitat),p(.) 0.00 0.468 Poecilotriccus plumbeiceps (.),p(habitat) 0.00 0.348 Platyrinchus mystaceus (habitat),p(.) 0.00 0.389 Lathrotriccus euleri (.),p(habitat) 0.00 0.474 Megarynchus pitangua (.),p(habitat) 0.00 0.347 Sirystes sibilator (habitat),p(.) 0.00 0.506 TITYRIDAE Schiffornis virescens (habitat),p(.) 0.00 0.640 Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Bird species Model ΔAICc AICc Weight CORVIDAE Cyanocorax chrysops (habitat),p(.) 0.00 0.556 TURDIDAE Turdus leucomelas (.),p(habitat) 0.00 0.468 THRAUPIDAE Trichothraupis melanops (habitat),p(.) 0.00 0.349 Conirostrum speciosum (.),p(.) 0.00 0.358 INCERTAE SEDIS Saltator similis (habitat),p(.) 0.00 0.317 PARULIDAE Setophaga pitiayumi (.),p(.) 0.00 0.412 Myiothlypis leucoblephara (.),p(habitat) 0.00 0.338 Basileuterus culicivorus (habitat),p(.) 0.00 0.480 ICTERIDAE Cacicus haemorrhous (habitat),p(habitat) 0.00 0.480 APPENDIX IV Bird species associated to river edge (RE) and forest interior (FI) habitats in the present study with their respective sensitivity to forest fragmentation (sensitive and non-sensitive) according to Anjos (2006) and Anjos et al. (2011). Bird species Sensitive Non-sensitive FI Crypturellus obsoletus X Trogon rufus X Pteroglossus castanotis X Hypoedaleus guttatus X Dysithamnus mentalis X Conopophaga lineata X Grallaria varia X Chamaeza campanisona X Dendrocolaptes platyrostris X Leptopogon amaurocephalus X Schiffornis virescens X Cyanocorax chrysops X Trichothraupis melanops X Basileuterus culicivorus X Phaethornis pretrei X Xiphorhynchus fuscus X Automolus leucophthalmus X Piprites chloris X Dacnis cayana X Pionopsitta pileata X Micrastur semitorquatus X Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Bird species Sensitive Non-sensitive Euphonia pectoralis X Picumnus temmincki X RE Melanerpes flavifrons X Xiphocolaptes albicollis X Capsiempis flaveola X Platyrinchus mystaceus X Sirystes sibilator X Saltator similis X Geotrygon montana X Colaptes melanochloros X Hylopezus nattereri X Lochmias nematura X Hemitriccus diops X Tolmomyias sulphurescens X Tityra cayana X Tachyphonus coronatus X Hemithraupis guira X Revista Brasileira de Ornitologia 27(3): 2019 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Bird species that occupy river edge in continuous forest tend to be less sensitive to forest fragmentation

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Abstract

Revista Brasileira de Ornitologia 27(3): 172–186. ARTICLE September 2019 Bird species that occupy river edge in continuous forest tend to be less sensitive to forest fragmentation 1,3 1 2 Barbara Rocha Arakaki Lindsey , Gabriela Menezes Bochio & Luiz dos Anjos Programa de Pós-Graduação em Ciências Biológicas, Universidade Estadual de Londrina, Londrina, PR, Brazil. Departamento de Biologia Animal e Vegetal, Laboratório de Ornitologia e Bioacústica, Universidade Estadual de Londrina, Londrina, PR, Brazil. Corresponding author: barbara.r.a.lindsey@gmail.com Received on 02 October 2018. Accepted on 21 August 2019. ABSTRACT: Along a distance gradient from a given river, two types of habitat can be recognized: natural river edge and forest interior, each one with its own vegetation characteristics and dynamics. In a continuous area of the Brazilian Atlantic Forest, we investigated (1) if bird communities are different between a riverbank of a small stream and an inland forest habitat; (2) if the species of the river edge habitat are the ones that persist in the most in forest fragments after deforestation of a continuous forest; (3) if the river edge habitat species are those that are less sensitive to forest fragmentation. It is expected that there are differences in the bird communities and the occupancy of some species between the two habitats. We allocated 16 sampling points in each of the habitats and sampled the birds by point counts with a short radius of 30 m. Results suggest that there is a significant difference between the composition of the bird communities of the river edge and forest interior habitats, although the species richness is similar. Six species were more likely to occupy the river edge and 14 species had a greater probability of occupancy in the forest interior. Species associated with the river edge habitat (15 species) tend not to be sensitive to forest fragmentation (12 species). In this study, we demonstrated that river-border species of continuous forest areas form a significant part of the bird communities that persist in small forest fragments, with intense edge effect. This shows that not all forest edge species are the result of the colonization from open areas. Congruently, species that occupy the most distant areas from the river vegetation in a continuous forest are those more sensitive to forest fragmentation. KEY-WORDS: Atlantic Rainforest, bird sensitivity, forest interior, natural edge, probability of occupancy. INTRODUCTION tree species; also, it is common to have the fall of trees and consequently the creation of clearings that allow the The Brazilian Atlantic Forest Biome, a tropical forest strip occupation of bamboo species (Bianchini et al. 2001, that stretches along 3300 km of the Brazilian coast beside Anjos et al. 2007). inland areas in Argentina and Paraguay, has thousands This lowland riparian environment constitutes a of endemic species (more than 650 species of vertebrates transition between the river and the associated upland and 8000 species of plants) and is considered one of forest, marking a natural border or ecotone boundary. A the key biodiversity hotspots in the world (Tabarelli et forest ecotone is a consequence of the meeting of distinct al. 2010, Mittermeier et al. 2011). The seasonal-semi- natural plant communities, which, in turn, influences the deciduous forest (SF), a type of forest in the Atlantic diversity of wild animals across the landscape, dependent Forest Biome, extends through the center-south of the on distance from a rivers' edge and the characteristic country interior, between 200 and 800 m of altitude and transition in topography, plant community, hydrological could be considered an ecoregion; there, approximately regimes, and soil types (Naiman et al. 1993, Shirley 2005). 220 tree species occur, 10% of which are endemic to this Considering several taxonomic groups, some studies forest type (Morellato & Haddad 2000, Oliveira-Filho & suggest greater species richness in riparian environments Fontes 2000, Scheer & Blum 2011, Anjos et al. 2018). compared to distinct forest (Naiman et al. 1993), others Locally in SF, many rivers, large and small, and streams found greater richness in non-riparian environments flow from upland areas to the lowland areas, as is common (McGaragal & McComb 1992, Peres 1997) and some along the Atlantic Forest. A distinct riparian environment found no difference between these two habitat types with a unique vegetative formation characterizes those (Gomez & Anthony 1998, Rykken et al. 2007). lowland river edges, which is the focus of the present On birds, several studies indicated the great study. This low land river edges forests usually has a importance of the riparian environment (natural river much less dense canopy with few emerging trees while edges) as a uniquely sustaining habitat with relatively more the under and midstory have a higher density of smaller species than associated upland forest areas (Woinarski Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. et al. 2000, Kajtoch et al. 2007, Dominguez-López & determined for the bird species of SF (see Anjos 2006, Anjos et al. 2011). The hypothesis is that the natural river Ortega-Álvarez 2014, Rannestad et al. 2015, Berduc et edge habitat species are the ones that persist in most of al. 2015, Sekercioglu et al. 2015, Gomez et al. 2016). In a tropical rainforest in Hong Kong, a higher number forest fragments in relation to the forest interior, after of individuals and bird species were recorded in the the deforestation of a continuous forest, that is, those riparian environment, when compared to an area 100– species are less sensitive to forest fragmentation. The reason for this hypothesis is that the vegetation of river 250 m distant from the river due to the high availability edges presents low trees and bushy entanglement in the of adult aquatic insects, which confirms the response of birds to river proximity (Chan et al. 2008). In a 656 lower stratum, phyto-physiognomy that resembles edges ha fragment of the Atlantic Forest in northern Paraná of forest fragments. state, with little topographic variation (~150 m altitude), Anjos et al. (2007) showed that 43% of all bird species METHODS were associated with riparian forest due to differences in vegetation; they sampled 81 species and found that 19 and 45 species were unique to the non-riparian and Study area riparian habitat, respectively. Another study conducted in The study was developed in the Iguaçu National the same site showed that the difference between the bird Park (INP), in the municipality of Céu Azul, Paraná communities is mainly due to the presence of bamboo in o o the riparian forest (Chusquea sp., Willrich et al. 2016). (25 09'12''S; 53 50'42''W, Fig. 1). INP was created in Therefore, riparian bir d species may comprise a significant 1939 and its total area is 185,262.2 ha; it is a fully protected proportion of the overall local forest bird richness and Conservation Unit whose predominant vegetation is SF (ICMBio 2014). In reality, INP is home to the country›s with particular traits associated to that vegetation closer largest continuous SF area. The INP climate, according to rivers. Riparian forest could be in some extension to the classification of Köppen, is of type Cfa subtropical comparable to edges of forest fragments, since both are humid or mesothermic with hot summer, with average ecotones. We argue that edge birds of riparian forest temperatures between 15 and 25 C and rainfall above 900 mm, also distributed throughout the year (Melo et should be more adapted to the edge of forest fragments, al. 2006). while birds inhabiting the interior of the forest avoid those created habitats after deforestation (Gimenes & Anjos SF is related, in virtually the whole area of occurrence, 2003, Hansbauer et al. 2008). In this study, we tested if to a climate of two well defined seasons - one rainy and it is possible that birds that originally live in the riparian one dry (Veloso et al. 1991). The vegetation is dense and presents a great variety of vegetal species, constituted by environment in the continuous forest could be more arboreal elements (perennial or deciduous), as well as tolerant to edges that appear after forest fragmentation. To do this, the first objective of this study was to verify shrub, lianas and epiphytes. Among tree species that are if bird communities are different between a natural river associated with SF are: Assai Palm (Euterpe edulis Mart.), edge habitat and a forest interior. For this, we investigated Peroba (Aspidosperma polyneuron Müll.Arg.), Brazilian Rosewood (Aniba rosaeodora Ducke), Alecrin (Holocalyx the richness and composition of the bird communities. balansae Micheli), Angico-cedro (Parapiptadenia rigida The hypothesis is that the richness and composition of the bird communities of the two habitats are different (Benth.) Brenan) and Argentine Cedar (Cedrela fissilis due to the difference of resour ces found in both habitats, Vell., Guimarães et al. 2003). e.g., the availability of adult aquatic insects in the river Sampling areas natural edge habitat and several resources (both animal and vegetal), associated to the river edge vegetation. The second o bjective of this study was to compare the We sampled two habitats and denominated them as occupancy of the bird species between the two habitats. “River Edge” and “Forest Interior”. The “River E dge” o o In this case, we evaluated the occupancy probability of the (RE; 25 09'43''S; 53 49'39''W) is located on the border of a tributary of the Azul River, and the “Forest Interior” bird species according to the different habitat types. The o o (FI; 25 09'28''S; 53 50'09''W) is located at 300 m of RE, occupancy of some bird species is expected to be different between the two types of habitat, due to differences in at higher altitude (565 m a.s.l.) and at 470 m of forest vegetation. The thir d objective of this study was to verify edge (Fig. 2 in Appendix I). The tributary of the Azul if the river natural edge habitat species are less sensitive to River is a small one, with 8 to 15 m width in the section studied. In each habitat, 16 points were established (Fig. forest fragmentation. In order to do this, we investigated 1). The shortest distance between RE and FI sampling the association between the number of bird species closely related with the river natural edge habitat and their points was 80 m. sensitivity to forest fragmentation, which was previously In RE, points were allocated in four tracks (REA, Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Figure 1. Location of Paraná state in South America and the region of the study in the Iguaçu National Park (INP), western Paraná, southern Brazil. The black dots indicate the location of the sample units (REA, REB, REC and RED in RE and FIA, FIB, FIC and FID in FI). the best-preserved parts, trunk with diameters at breast height (DBH) of more than 1 m (ICMBio 1999). Bird sampling We used the point count method with radius of 30 m (Bibby et al. 1993) in bird sampling. This method is very effective in studies of avian habitat relationships (Anjos et al. 2010). Sampling was carried out during the breeding season of January and February of 2013, in which birds are more likely to be detected by the observer through their vocalizations. Each set of four points in both habitats was Figure 2. Non-metric multidimensional scaling (NMDS) of considered as a sample unit, which was sampled in one bird communities in eight different sample units (REA, REB, day. These sample units were named REA, REB, REC REC, RED, FIA, FIB, FIC, and FID) occurring in two habitats and RED in RE and FIA, FIB, FIC and FID in FI. On (“River Edge” and “Forest Interior”) at INP. each day the points of each sample unit were sampled consecutively 1, 2, 3 and 4, and then again reversing REB, REC and RED), perpendicular to the river. The the sequence, 4, 3, 2 and 1. For example, on track A trails in this habitat were at least 300 m apart (Fig. 2 In in RE, on one day the sampling sequence of the points Appendix I). In FI, the points were allocated on a trail of was REA1, REA2, REA3, REA4, REA4, REA3, REA2, 1200 m located inside the forest. The 16 points located in REA1. The following day the sampling sequence of the this track were subdivided into four blocks of four points points was reversed: REA4, REA3, REA2, REA1, REA1, (blocks FIA, FIB, FIC, FID, Fig. 3 in Appendix I). REA2, REA3, REA4. We sampled each sampling unit for In RE habitat we observe lower trees, with a height two days, and we sampled each sampling point four times of 8 to 15 m, having less plant species richness. Also, the (as if they had been sampled on four mornings). Studies species are adapted to periodic flooding which supports performed in the Atlantic Forest using the point count high humidity (ICMBio 1999). In the transition from RE method demonstrated that 3 to 5 days of sampling are habitat to IF habitat, vegetation changes and trees become sufficient to detect more than 90% of the species recor ded taller. In the FI habitat there is a greater richness of plant in a sample area (Anjos 2007, Cavarzere et al. 2013). species; there are large trees, with maximum heights of Sampling began shortly after sunrise, when daytime 35 m in the emerging layer, and it is common to find in birds start to vocalize, and ended 2.5 h after sampling at Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. the first point, under favorable climatic conditions. We is the probability of the species being present in one place, sampled each point for 10 min with a 10 min interval and the probability of detection (p). between points. According to Anjos et al. (2010), if the Single season occupancy modeling requires multiple observer is interested in assessing differences between visits to sampling units during a season in which species numbers of bird species at different locations, the time can be detected. This model assumes that during these of 10 min is sufficient and in SF, 96% of the species are visits no individual enters or leaves the population (closed recorded during this time interval. model). At each visit the observer detects the presence (“1”) or absence (“0”) of the species of interest. The Statistical analysis absence may be a real absence of the species or a failure to detect the species. This type of modeling adjusts the We estimated the total richness of the bird species using variation in probability of detection while estimating the the non-parametric Chao species estimator (Herzog probability of occupancy of bird species. By incorporating et al. 2002). We evaluated the influence of space the probability of detection into the models, the imperfect (spatial autocorrelation) on the composition of bird detection is considered and the bias in the parameter species through the Mantel test (1000 permutations). estimation is reduced (MacKenzie et al. 2006). The geographic distance matrix was obtained by the Since each point was sampled four times, in each Euclidean distance on the geographical coordinates of sampling we recorded if each species of bird was detected the sample units. We obtained the similarity matrix of or not. Thus, the detection history for each bird species the species composition using the distance of Bray Curtis in each area was obtained. The detection history was on the abundance of the species in each sample unit. We then used to estimate the probability of occupancy of the performed the analysis in R software (R Development species. Core Team 2015), using the package “vegan” (Legendre For this model, the estimated parameters (occupancy & Legendre 1998, Oksanen et al. 2016). and detectability) may be a function of covariates. The We estimated the relative abundance for a single PRESENCE software (Hines 2006) recognizes two species in a habitat (RE or FI), called the Index of Point types of covariates, (1) site-specific covariates, which are Abundance (IPA), by dividing its contact number by constant for the site within the same season, e.g., habitat the total number of points sampled in each site (Bibby type, fragment size, or generalized weather patterns, et al. 1993). To avoid double counting for the same such as drought or El Niño; and (2) sampling-occasion individuals' precautions were taken particularly for those covariates, which may vary at each sampling, such as highly mobile species by adopting a field form that is temperature, precipitation, time of day or observer divided into different quadrants as suggested by Vielliard (Hines 2006). In order to verify the probability of & Silva (1990). Thus, a number of contacts of 30 for occupation of the bird species in each of the habitats, a given species resulted in an IPA equal to 0.468 (30 in the present study the first type of covariant was used. contacts divided by 64 points sampled). Thus, we tested w hether the probability of occupancy of To verify differences in bir d species composition each species of bird occurred as a function of habitat. We between the two habitats we used a permutational analysis ran occupancy models which assumed that the occupancy of variance (PERMANOVA) (Anderson 2001). This and detection of the species were constant - null models analysis was performed in R software (R Development (e.g., same probability of occurrence among all points Core Team 2015), using the packages “vegan” (Oksanen sampled), models that assumed that the probability et al. 2016) and “BiodiversityR” (Kindt & Coe 2005). of species occupancy was in function of the covariant We used non-metric multidimensional scaling habitat, models that assumed that species detection was (NMDS) to visualize the similarity in community a function of covariant habitat and models who assumed composition between the two habitats (Clarke 1993). that the probability of species occupancy and species Data was transformed through weighting dispersion to detection was in function of the covariant habitat. reduce the contribution of high abundance species in We used the Akaike Information Criterion (AIC, the similarity. Similarities of Bray-Curtis were used to Burnham & Anderson 2002) for small sample sizes construct the distance matrices between sample units. (AICc), to select the most parsimonious model. The best This analysis was performed using software PRIMER v. 6 models were those with lower AICc values and higher (Clarke & Gorley 2006). AICc weights; the closer to 1 the AICc weight value, the For each bird species recorded in both habitats, we greater the likelihood of the model being chosen as the calculated the probability of occupancy in the different best (Burnham & Anderson 2002). This analysis was habitats using single-season occupancy modeling performed using PRESENCE 9.0 software (Hines 2006). (MacKenzie et al. 2002). These models involve t he We used a contingency table to investigate the estimation of two parameters: the occupancy (Y), which relationship between the number of birds associated Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. with RE and IF habitats with their sensitivity to forest campanisona, Dendrocolaptes platyrostris, Leptopogon fragmentation (sensitive and non-sensitive). The bir d amaurocephalus, Schiffornis virescens, Cyanocorax chrysops, species' level of sensitivity used was presented in Anjos Trichothraupis melanops, Basileuterus culicivorus). (2006) and Anjos et al. (2011). Anjos (2006) determined Considering the set of species analyzed, 15 bird the sensitivity of the birds to forest fragmentation in SF species were more associated to RE habitat, of which based on samplings carried out in 14 forest fragments three are sensitive and 12 are not sensitive to forest of different sizes and degrees of isolation. Species were fragmentation. Twenty-three bird species were more considered sensitive if they occurred only in control associated to FI habitat, of which 14 are sensitive and 9 fragments or in large, non-isolated fragments; species are not sensitive to forest fragmentation (Appendix IV). not sensitive to forest fragmentation were those that Thus, the data suggest that species of birds susceptible to occurred in all fragments, including the smallest and habitat fragmentation were those associated with the FI most isolated ones (Anjos 2006). In the present study we habitat while those that are not sensitive to fragmentation used two criteria to determine if a given species of bird were those associated with RE habitat ( = 6.13; P = was associated with one of the habitats, RE or FI: 1) the 0.013). species should be exclusive to one habitat and with at least three contacts during the total sampling period; or 2) the species should have a higher probability of occupancy in DISCUSSION one of the habitats. The software Past 3.0 was used to calculate the contingency table (Hammer et al. 2001). We found a significant difference between the The taxonomy and nomenclature followe d American composition of the bird communities of RE and FI Ornithologists' Union - South American Classification habitats, although the species richness was similar. The Committee Checklist for South American Birds (SACC; difference in the composition was due to several exclusive Remsen-Jr. et al. 2016). species in each habitat and to several species that occurred in both habitats but which showed greater occupancy in only one habitat. Species associated with the RE habitat RESULTS tend not to be sensitive to forest fragmentation. In the study by Anjos (2006) on the sensitivity of birds to forest We recorded a total of 80 species of birds in both fragmentation, species that present tolerance to edges habitats, similar to the estimated richness (Chao , 84 ± showed low sensitivity to fragmentation. The results 4 species). We detected no autocorrelation between the of the present study indicate that of the total species geographical distances of the sample units and the species associated to the RE habitat, only 20% are sensitive to composition (Mantel r = 0.063, P = 0.320). We recorded forest fragmentation, while 61% of the species associated 65 bird species in RE and 68 in FI. The number of species to the FI habitat are sensitive to forest fragmentation estimated by Chao for RE was 70 ± 4 species and the (Appendix IV). estimated number for FI was 79 ± 6 species. Therefore, A large number of physical and biological processes we found no difference between the estimated richness of occur from the edge of a fragment because of the influence the two habitats. Twelve species were recorded only in RE of the matrix habitat (Laurance et al. 2011). This influence and 15 were exclusive to FI (Appendix II). on physical and biological processes occurs up to 200– The composition of bird communities differed 500 m from the border into the fragment (Laurance et al. between habitats (PERMANOVA, Pseudo-F = 6.785, P 2011). Therefore, small and/or very elongated fragments < 0.010). In concordance with this result, the ordering are “all edge”, that is, without an interior free of edge of the NMDS showed that the RE and FI sample units effects. These processes can affect forest bir d species. differ in composition and a bundance of bird species, as Species associated with FI, such as Micrastur semitorquatus, they were grouped separately (Fig. 2). Automolus leucophtalmus, Grallaria varia and Schiffornis Among the 53 species that occurred both in RE virescens do not occur in fragments smaller than 60 ha; and FI, the habitat type influenced t he probability of on the other hand, of the 15 species associated with RE, occupancy of 20 species (Appendix III). Six species had about 67% persist in small forest fragments of 11 and a higher probability of occupancy in RE (Melanerpes 25 ha (Anjos 2001). We should highlight that non-forest flavifrons, Xiphocolaptes albicollis, Capsiempis flaveola, colonizer bird species occur in the edge of forest fragments. Platyrinchus mystaceus, Sirystes sibilator, Saltator similis) Those are species from open and/or Cerrado areas, such as and 14 species showed a higher probability of occupation Rupornis magnirostris, Colaptes melanochloros, Melanerpes in FI (Crypturellus obsoletus, Trogon rufus, Pteroglossus candidus, Patagioenas maculosa and Myiarchus swainsoni castanotis, Hypoedaleus guttatus, Dysithamnus mentalis, (Anjos 2001, Baptista et al. 2016, Bierregaard et al. 2016, Conopophaga lineata, Grallaria varia, Chamaeza Joseph 2016, Winkler et al. 2016). Thus, the composition Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. of birds of the edge of a forest fragment should originate by invertebrates (Wilman et al. 2014). Populations at mainly from those living on river banks in continuous the edge of their geographical distribution are generally forest combined with those colonizers from open areas. smaller than those closest to the center of the geographical However, some species of interior forest can also persist in distribution (Holt et al. 2005). The INP is situated on the fragments. Anjos (2001) studied the bird community the southern edge of the geographical distribution of T. in small forest fragments (56, 25 and 11 ha in size). Based coronatus. It is possible that the population of T. coronatus on the present study and in Anjos et al. (2007), we found in the INP is smaller than the population of the species that the majority of the bird species that live in these at the site studied by Cândido-Jr. (2000). Perhaps in small fragments are species that inhabit river bank and/or INP the individuals of this species were concentrated in are colonizing species: 80% in FA, 82% in FB and 84% the habitat RE due to greater availability of some type in FC. of resource or even by competition and the presence of Fragmentation and habitat degradation cause predators. changes in the forest edge, such as increased temperature In this study we demonstrated that river-edge bird and light intensity. In Neotropical forests, birds that live species of a continuous area of forest form a significant on riverbanks in a continuous forest and occupy the edge part of the bird communities that persist in small forest of the remaining habitat after fragmentation and birds fragments, with intense edge effect. This shows that not from open areas should select similar abiotic conditions all the forest edge species are the result of colonization such as air temperature, spatial variation of solar from open habitats. As expected, species that occupy the radiation, humidity and wind speed. On the other hand, most remote areas of the river vegetation in a continuous forest species, such as understory insectivorous birds, forest are those most sensitive to forest fragmentation. select microhabitats with different abiotic characteristics and do not occupy the edge of the small forest fragments or fragments considered “all border” (Pollock et al. 2015, ACKNOWLEDGEMENTS Stratford & Stouffer 2015). In fact, birds associated with darker microhabitats are more sensitive to forest edge This study was funded in part b y the Coordenação de than birds that use brighter microhabitats (Patten & Aperfeiçoamento de Pessoal de Nível Superior - Brasil Smith-Patten 2012). However, the forest interior is also (CAPES) - B.R.A.L. received CAPES “sandwich doctorate” home to several sensitive species to forest fragmentation, scholarship (99999.012747/2013-00) and G.M.B. which are not particularly associated to forest understory, received CAPES “sandwich doctorate” scholarships such as Pionopsitta pileata, one of the most threatened (99999.012746/2013-04). L.d.A. received financial species of psittacines due to the massive destruction of support from CNPq (Brazilian Council for Development their habitat (Sigrist 2013), which occurred exclusively of Science and Technology, Brasilia; 306293/2014-5). in the FI habitat. It is important to point out that in RE Chico Mendes Institute for Conservation of Biodiversity there were also species that were exclusive of that habitat (ICMBio, Brasilia) gave us permission (36241-2) to study and are sensitive to forest fragmentation, such as Coccyzus birds in the Iguaçu National Park, where we had the melacoryphus, Hylopezus nattereri and Tityra cayana. The assistance of PIC Ceu Azul staff. We t hank J.M. Lindsey, reason of these species' sensitivity may be related to the a native speaker from the United States, for English vegetation structure, or even the lower humidity of the proofreading. K. Sieving provided helpful comments and edges of a fragment compared to the river's edge (Pollock suggestions for this manuscript. et al. 2015). 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Sites sampled in the INP: A) “River Edge”, on the edge of a tributary of the Azul River, and B) “Forest Interior”. Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Figure 2. The four points of each of the trails (REA, REB, REC and RED) in the River E dge habitat sampled at INP. Figure 3. The four blocks (FIA, FIB, FIC and FID) of four points located on the trail of FI habitat at INP. APPENDIX II Families and bird species sampled in RE and FI habitats at INP. Taxonomy follows American Ornithologists' Union - South American Classification Committee Checklist for South American Bir ds (Remsen-Jr. et al. 2016). Presence Bird species RE FI TINAMIDAE Crypturellus obsoletus XX Crypturellus parvirostris X Crypturellus tataupa XX COLUMBIDAE Patagioenas picazuro XX Geotrygon montana X Leptotila verreauxi X CUCULIDAE Piaya cayana XX Coccyzus melacoryphus X TROCHILIDAE Phaethornis pretrei X Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Presence Bird species RE FI TROGONIDAE Trogon surrucura XX Trogon rufus XX MOMOTIDAE Baryphthengus ruficapillus XX RAMPHASTIDAE Ramphastos dicolorus XX Selenidera maculirostris XX Pteroglossus castanotis XX PICIDAE Picumnus temminckii X Melanerpes flavifrons XX Colaptes melanochloros X Dryocopus lineatus XX Campephilus robustus XX FALCONIDAE Micrastur semitorquatus X Milvago chimachima X PSITTACIDAE Pionopsitta pileata X Pionus maximiliani XX Pyrrhura frontalis XX Psittacara leucophthalmus XX THAMNOPHILIDAE Hypoedaleus guttatus XX Mackenziaena severa XX Thamnophilus caerulescens XX Dysithamnus mentalis XX Herpsilochmus rufimarginatus XX Drymophila rubricollis X Drymophila malura XX Pyriglena leucoptera XX CONOPOPHAGIDAE Conopophaga lineata XX GRALLARIIDAE Grallaria varia XX Hylopezus nattereri X RHINOCRYPTIDAE Eleoscytalopus indigoticus XX FORMICARIIDAE Chamaeza campanisona XX Chamaeza meruloides XX Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Presence Bird species RE FI FURNARIIDAE Sittasomus griseicapillus XX Dendrocincla fuliginosa XX Dendrocolaptes platyrostris XX Xiphocolaptes albicollis XX Xiphorhynchus fuscus X Lochmias nematura X Anabacerthia lichtensteini XX Automolus leucophthalmus X Synallaxis ruficapilla XX TYRANNIDAE Myiopagis caniceps XX Camptostoma obsoletum XX Capsiempis flaveola XX Leptopogon amaurocephalus XX Hemitriccus diops X Poecilotriccus plumbeiceps XX Tolmomyias sulphurescens X Platyrinchus mystaceus XX Lathrotriccus euleri XX Pitangus sulphuratus X Myiodynastes maculatus X Megarynchus pitangua XX Sirystes sibilator XX TITYRIDAE Tityra cayana X Schiffornis virescens XX INCERTAE SEDIS Piprites chloris X CORVIDAE Cyanocorax chrysops XX TURDIDAE Turdus leucomelas XX THRAUPIDAE Cissopis leverianus X Trichothraupis melanops XX Tachyphonus coronatus X Dacnis cayana X Hemithraupis guira X Conirostrum speciosum XX INCERTAE SEDIS Saltator similis XX Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Presence Bird species RE FI CARDINALIDAE Habia rubica X PARULIDAE Setophaga pitiayumi XX Myiothlypis leucoblephara XX Basileuterus culicivorus XX ICTERIDAE Cacicus haemorrhous XX Cacicus haemorrhous XX FRINGILLIDAE Euphonia pectoralis X APPENDIX III Best models tested for occupancy probability as a function of the different habitat types (RE and FI) at INP, for the bird species that occurred in both habitats. Occupancy (); Probability of detection (p); Difference between the AICc models (ΔAICc). Taxonomy follows American Ornithologists' Union - South American Classification Committee Checklist for South American Birds (Remsen-Jr. et al. 2016). Bird species Model ΔAICc AICc Weight TINAMIDAE Crypturellus obsoletus (habitat),p(.) 0.00 0.40 Crypturellus tataupa (.),p(habitat) 0.00 0.357 COLUMBIDAE Patagioenas picazuro (.),p(.) 0.00 0.386 CUCULIDAE Piaya cayana (.),p(.) 0.00 0.362 TROGONIDAE Trogon surrucura (.),p(habitat) 0.00 0.317 Trogon rufus (habitat),p(.) 0.00 0.448 MOMOTIDAE Baryphthengus ruficapillus (.),p(habitat) 0.00 0.404 RAMPHASTIDAE Ramphastos dicolorus (.),p(.) 0.00 0.459 Selenidera maculirostris (.),p(.) 0.00 0.389 Pteroglossus castanotis (habitat),p(.) 0.00 0.523 PICIDAE Melanerpes flavifrons (habitat),p(.) 0.00 0.369 Dryocopus lineatus (.),p(.) 0.00 0.402 Campephilus robustus (.),p(.) 0.00 0.358 (.),p(habitat) 1.34 0.183 (habitat),p(habitat) 2.57 0.099 Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Bird species Model ΔAICc AICc Weight PSITTACIDAE Pionus maximiliani (.),p(.) 0.00 0.518 (.),p(habitat) 2.48 0.187 (habitat),p(habitat) 4.59 0.034 Pyrrhura frontalis (.),p(.) 0.00 0.323 Psittacara leucophthalmus (.),p(.) 0.00 0.298 THAMNOPHILIDAE Hypoedaleus guttatus (habitat),p(.) 0.00 0.486 Mackenziaena severa (.),p(.) 0.00 0.417 Thamnophilus caerulescens (.),p(.) 0.00 0.358 Dysithamnus mentalis (habitat),p(.) 0.00 0.617 Herpsilochmus rufimarginatus (.),p(.) 0.00 0.502 Drymophila malura (.),p(.) 0.00 0.293 Pyriglena leucoptera (.),p(.) 0.00 0.284 CONOPOPHAGIDAE Conopophaga lineata (habitat),p(.) 0.00 0.482 GRALLARIIDAE Grallaria varia (habitat),p(.) 0.00 0.439 RHINOCRYPTIDAE Eleoscytalopus indigoticus (.),p(habitat) 0.00 0.270 FORMICARIIDAE Chamaeza campanisona (habitat),p(.) 0.00 0.593 Chamaeza meruloides (.),p(.) 0.00 0.3586 FURNARIIDAE Sittasomus griseicapillus (.),p(habitat) 0.00 0.486 Dendrocincla fuliginosa (.),p(.) 0.00 0.376 Dendrocolaptes platyrostris (habitat),p(.) 0.00 0.461 Xiphocolaptes albicollis (habitat),p(.) 0.00 0.360 Anabacerthia lichtensteini (.),p(.) 0.00 0.441 Synallaxis ruficapilla (.),p(.) 0.00 0.485 TYRANNIDAE Myiopagis caniceps (.),p(.) 0.00 0.450 Camptostoma obsoletum (.),p(.) 0.00 0.407 Capsiempis flaveola (habitat),p(.) 0.00 0.468 Leptopogon amaurocephalus (habitat),p(.) 0.00 0.468 Poecilotriccus plumbeiceps (.),p(habitat) 0.00 0.348 Platyrinchus mystaceus (habitat),p(.) 0.00 0.389 Lathrotriccus euleri (.),p(habitat) 0.00 0.474 Megarynchus pitangua (.),p(habitat) 0.00 0.347 Sirystes sibilator (habitat),p(.) 0.00 0.506 TITYRIDAE Schiffornis virescens (habitat),p(.) 0.00 0.640 Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Bird species Model ΔAICc AICc Weight CORVIDAE Cyanocorax chrysops (habitat),p(.) 0.00 0.556 TURDIDAE Turdus leucomelas (.),p(habitat) 0.00 0.468 THRAUPIDAE Trichothraupis melanops (habitat),p(.) 0.00 0.349 Conirostrum speciosum (.),p(.) 0.00 0.358 INCERTAE SEDIS Saltator similis (habitat),p(.) 0.00 0.317 PARULIDAE Setophaga pitiayumi (.),p(.) 0.00 0.412 Myiothlypis leucoblephara (.),p(habitat) 0.00 0.338 Basileuterus culicivorus (habitat),p(.) 0.00 0.480 ICTERIDAE Cacicus haemorrhous (habitat),p(habitat) 0.00 0.480 APPENDIX IV Bird species associated to river edge (RE) and forest interior (FI) habitats in the present study with their respective sensitivity to forest fragmentation (sensitive and non-sensitive) according to Anjos (2006) and Anjos et al. (2011). Bird species Sensitive Non-sensitive FI Crypturellus obsoletus X Trogon rufus X Pteroglossus castanotis X Hypoedaleus guttatus X Dysithamnus mentalis X Conopophaga lineata X Grallaria varia X Chamaeza campanisona X Dendrocolaptes platyrostris X Leptopogon amaurocephalus X Schiffornis virescens X Cyanocorax chrysops X Trichothraupis melanops X Basileuterus culicivorus X Phaethornis pretrei X Xiphorhynchus fuscus X Automolus leucophthalmus X Piprites chloris X Dacnis cayana X Pionopsitta pileata X Micrastur semitorquatus X Revista Brasileira de Ornitologia 27(3): 2019 River's edge birds are less sensitive to forest fragmentation Lindsey et al. Bird species Sensitive Non-sensitive Euphonia pectoralis X Picumnus temmincki X RE Melanerpes flavifrons X Xiphocolaptes albicollis X Capsiempis flaveola X Platyrinchus mystaceus X Sirystes sibilator X Saltator similis X Geotrygon montana X Colaptes melanochloros X Hylopezus nattereri X Lochmias nematura X Hemitriccus diops X Tolmomyias sulphurescens X Tityra cayana X Tachyphonus coronatus X Hemithraupis guira X Revista Brasileira de Ornitologia 27(3): 2019

Journal

Ornithology ResearchSpringer Journals

Published: Sep 1, 2019

Keywords: Atlantic Rainforest; bird sensitivity; forest interior; natural edge; probability of occupancy

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