Emu - Austral Ornithology

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Bird species richness, composition and abundance in pastures are affected by vegetation structure and distance from natural habitats: a single tree in pastures matters Mauricio Neves Godoi, Rudi Ricardo Laps, Danilo Bandini Ribeiro, Camila Aoki & Franco Leandro de Souza To cite this article: Mauricio Neves Godoi, Rudi Ricardo Laps, Danilo Bandini Ribeiro, Camila Aoki & Franco Leandro de Souza (2017): Bird species richness, composition and abundance in pastures are affected by vegetation structure and distance from natural habitats: a single tree in pastures matters, Emu - Austral Ornithology To link to this article: https://doi.org/10.1080/01584197.2017.1398591

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Date: 21 November 2017, At: 03:28

EMU - AUSTRAL ORNITHOLOGY, 2017 https://doi.org/10.1080/01584197.2017.1398591

Bird species richness, composition and abundance in pastures are affected by vegetation structure and distance from natural habitats: a single tree in pastures matters Mauricio Neves Godoi

a

, Rudi Ricardo Lapsb, Danilo Bandini Ribeirob, Camila Aokic and Franco Leandro de Souzab

a

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Ecology and Conservation, Center of Biological and Health Sciences, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil; bCenter of Biological and Health Sciences, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil; cFederal University of Mato Grosso do Sul, Aquidauana, Mato Grosso do Sul, Brazil ABSTRACT

ARTICLE HISTORY

Throughout the world, natural habitats have been replaced by pastures. Thus, bird conservation requires making pastures more accessible for birds. The use of pastures by birds inhabiting the surrounding natural habitats may be affected by the structure of pastures and their distance from natural habitats. In this study we tested whether bird species richness, composition and abundance in pastures of the Brazilian Cerrado are linked to habitat and dietary requirements and affected by vegetation structure and the distance to natural habitats. We found that pastures with more trees and shrubs had greater richness of forest birds, forest insectivorous birds and semi-forest insectivorous-frugivorous birds. Pastures with taller trees had greater richness of semiforest insectivorous birds, and pastures closer to natural habitats had greater richness of forest frugivorous birds. Bird composition in pastures changed according to vegetation structure and distance from natural habitats, and the abundance of some bird species was positively correlated to vegetation structure and negatively correlated to distance from natural habitats. These findings highlight the importance of trees and shrubs in pastures and maintaining patches of natural habitats near pastures. Management measures can make pastures more accessible for birds from surrounding natural environments and could help in bird conservation.

Received 2 August 2016 Accepted 13 October 2017

Introduction Natural habitats have been modified and converted for human use throughout the world, but especially for the expansion of pastures and crop areas (Myers et al. 2000; Laurance et al. 2014). In the Brazilian Cerrado – a large phytogeographic domain comprising a mosaic of forests, savannas and natural grasslands – pastures and crop areas already occupy more than 53% of the landscape (Klink and Machado 2005), replacing natural habitats where more than 850 bird species live (Silva and Bates 2002; Silva and Santos 2005). Since extensive patches of natural habitats are becoming increasingly rare as a result of their rapid replacement with pastures and crop areas, the conservation of native bird species depends not only on maintaining the remaining natural habitats but also on their ability to forage successfully and move across these modified landscapes (Harvey et al. 2006; Mendoza et al. 2014). Therefore, these areas need to be managed so that they can better provide the habitats CONTACT Mauricio Neves Godoi [email protected] Supplemental data for this article can be accessed here. © 2017 BirdLife Australia

KEYWORDS

Avian communities; bird conservation; Bodoquena Mountains; Cerrado domain; pasture management

and resources that native bird species require. This management would also facilitate bird movement across this anthropised matrix by increasing connectivity between populations that persist in the remaining natural habitats (Harvey et al. 2006; Mendoza et al. 2014). Such management of pastures and crops can benefit birds, which in turn can support human economic activities. Native birds perform important functions in ecosystems, many of which can have positive influences on the human economy, such as pest control and aiding the recovery of degraded areas via seed dispersal (Sekercioglu et al. 2004; Sekercioglu 2006). One way to make pastures and crops more accessible for birds is to increase the complexity of their vegetation. Increasing complexity can result in an increase in bird species richness and abundance, and changes to bird community composition (Tews et al. 2004; Jayapal et al. 2009; Jankowski et al. 2012). In addition, vegetation structure affects birds of a wide variety of trophic groups. For example, species richness, composition and abundance of insectivorous and frugivorous birds can be

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affected by tree and shrub densities, tree height and canopy cover, among many other components of vegetation structure (Cueto and De Casenave 2000; Hasui et al. 2007; Ding et al. 2008; Laube et al. 2008; Jayapal et al. 2009; Jankowski et al. 2012). Landscapes dominated by pastures and crops can maintain a greater richness of bird species, including forest birds, when vegetation complexity is maintained, such as through the retention of riparian forests and forest patches (Estrada et al. 1997; Petit et al. 1999; Wilson et al. 2005; Harvey et al. 2006; Mendoza et al. 2014). Even isolated trees can make pastures and crops more accessible for birds because they add complexity to vegetation structure and provide resources and habitats that forest bird species require, thereby facilitating increased mobility across the landscape (Estrada et al. 2000; Fischer and Lindenmayer 2002; Naidoo 2004; Harvey et al. 2006; Laube et al. 2008; Mendoza et al. 2014). Another important factor in maintaining forest bird richness in pastures and crop areas is the distance from natural habitats (Luck and Daily 2003; Naidoo 2004; Laube et al. 2008). Studies have shown that species richness of forest birds tends to be greater in pastures and crops closer to natural habitats (Naidoo 2004; Laube et al. 2008). Furthermore, some groups of birds that are more sensitive to forest fragmentation, such as frugivorous forest species, also exhibit greater richness in pastures and crops that are closer to natural habitats (Luck and Daily 2003; Laube et al. 2008). Despite the importance of understanding how pastures and crops can be more accessible for bird species and particularly for forest species (Laube et al. 2008; Mendoza et al. 2014), this topic has been poorly studied in the Cerrado domain. The Cerrado domain is considered a hotspot of biodiversity (Myers et al. 2000), yet it is one of the most threatened phytogeographic domains in the world due to the expansion of cattle ranching and agriculture (Klink and Machado 2005). A few studies have addressed the effects of vegetation structure on birds that occur in Cerrado pastures. Tubelis and Cavalcanti (2000), for example, have shown that pastures with more shrubs had greater bird species richness and different species composition than pastures with few shrubs. In the Bodoquena Mountains of the Cerrado of western Brazil, Godoi et al. (2016) studied bird communities in a forest– savanna–pasture gradient, and found that pastures with greater tree and shrub density (dirty pastures) had different compositions of birds than did pastures with lower tree and shrub density (clean pastures). These dirty pastures had bird communities more similar to the surrounding woodland savannas, and were capable of harbouring many forest and semi-forest bird

species, as opposed to clean pastures, which were used mainly by open-area birds. Although these studies have pointed out the importance of tree and shrub density to birds in pastures, they lack information about the importance of the specific elements of vegetation structure provided by the presence of native plants. Tree height and canopy cover, for example, are important elements of vegetation structure that can affect pasture bird communities (Laube et al. 2008). These studies also did not address how bird species of different trophic groups respond to vegetation structure in pastures, nor did they explore the effects of the distance of pastures from natural habitats on bird communities. In this study, we tested the hypothesis that birds from different habitats and trophic groups that occur in pastures are affected by vegetation structure and distance from natural habitats. Specifically, we made the following predictions: (1) species richness of forest and semi-forest birds, as well as the richness of their main trophic groups (insectivorous, frugivorous and insectivorous-frugivorous birds), should be greater in pastures closer to natural habitats and in those with greater structural complexity of their vegetation (i.e. more trees and shrubs, and taller trees and greater canopy cover); and (2) the species composition and abundances of forest and semi-forest birds in pastures should be correlated with the number of trees and shrubs, tree height, canopy cover and the distance from natural habitats.

Materials and methods Study area This study was carried out in the Bodoquena Mountains in western Brazil (Figure S1, supplementary material). The mean altitude of the region ranged from 400 to 600 m above sea level, with maximum values around 770 m and minimum values around 300 m (ICMBIO 2013). The climate is Aw, or Tropical Savanna, according to the Köppen classification, with mean annual temperatures between 22 and 26°C, maximum temperatures ranging from 35 to 40°C, and minimum temperatures reaching near 0°C. Air humidity is low, rarely reaching 80%, and mean annual precipitation is 1400 mm, with a wet season from November to March, and a dry season from April to October (IBGE 2006). The landscape of the Bodoquena Mountains comprises a mosaic of forests, savannas, natural grasslands and anthropogenic areas, which includes pastures for cattle ranching and soybean monocultures (Pott and

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Pott 2003). Biogeographically, the region is located in a transition between the Cerrado and Pantanal domains, but is also influenced by the Atlantic Forest and Chaco domains (Veloso et al. 1991). Study sites were located within the ‘Reserva Particular do Patrimônio Natural (RPPN) Estância Mimosa’, as well as in surrounding areas (EM hereafter), with a total study area of 8 km2 (800 ha) (Figure S1, supplementary material). The RPPN is a type of private reserve recognised by Brazilian environmental law. In EM, there are pastures and extensive patches of natural habitat of riparian forests, seasonal forests, woodland savannas (cerradão – forested savannas with high tree density and continuous canopy cover, with trees that are more than 8 m in height) and arboreal savannas (cerrado – savannas with scattered trees, high shrub density and with trees that usually have less than 8 m in height). Cattle ranching, one of the main economic activities of the region, is developed within EM as a silvopastoral system, with pastures varying in the extent of arboreal and shrubby cover, and which are often small and surrounded by large patches of natural habitats. Data collection The study area was divided into 280 grids of 200 m × 200 m, of which 200 were randomly selected, each of which was considered a sampling unit, encompassing all vegetation types of EM (Godoi et al. 2016). Of these, 84 were located in anthropogenic pastures, which occupy about 3.42 km2 (342 ha) widely distributed throughout the study area (Figure S1, supplementary material). During 12 consecutive months, from July 2011 to June 2012, we collected data on bird occurrence, vegetation structure (number of trees and shrubs, tree height and canopy cover) and distance to natural habitats for the 84 sampling units located in pastures. In order to sample birds we established a point in the centre of each of the 84 sampling units with a fixed radius of 50 m (Bibby et al. 1992). The distance between sampling units ranged from 200 to 4250 m, with an average of 1554 m. All sampling units had the same sampling effort and were visited only once during the study for 15 min, always in the early morning, between 0600 and 0830h, when most bird species were active. For each point we recorded all birds that were foraging (excluding birds that were flying across the point), noting species identity, species richness and abundance (number of individuals for each bird species). Although each sampling unit was visited only once during the study, comparisons between them can be made because they were sampled with the

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same methodology and sampling effort. Besides that, we excluded from our statistical analysis the migratory birds, according to Nunes and Tomas (2008), since they can cause differences in bird richness, abundance and composition between sampling units visited in different periods of the year. Pasture vegetation structure was characterised by collecting vegetation data in five 4 m × 4 m plots placed 10 m apart from one another in each sampling unit. The following data were recorded for each unit: (1) the number of trees with diameter at breast height (DBH) ≥ 10 cm, and the number of shrubs (woody plants with DBH ≤ 10 cm and height ≤ 4 m), which were counted individually in the five plots; (2) tree height (mean height of the five tallest trees, one per plot, with height being estimated visually); and (3) canopy cover (mean percentage of canopy cover based on five measurements, one in each plot, which were made by determining the number of a possible one hundred 5 cm × 5 cm squares of a 0.5 m x 0.5 m square grid that were covered by vegetation of the tree canopy). The distance between pastures and natural habitats was determined by measuring the distance between the centre of each sampling unit and the closest patch of natural habitat using images from Google Earth for the same year as when the bird data were collected. Data analysis In the present study, forest and semi-forest birds were considered to be those species that are dependent or semi-dependent on forested habitats, respectively, according to Stotz et al. (1996) and Bregman et al. (2014). Bird species were also classified according to their diet following Wilman et al. (2014), with the addition of information from field observations and our own experience with the natural history of the bird species considered. The main trophic groups of the birds studied at EM were insectivores (insects are the main food item), frugivores (fruits are the main food item) and insectivores-frugivores (insects and fruits are equally important food items). The taxonomic classification and nomenclature for the birds in this study follow the Brazilian Ornithological Records Committee (CBRO 2014). To determine whether there was spatial autocorrelation among sampling units, a Mantel test with 10 000 randomisations was used, testing the relationship between species composition dissimilarities and geographic distance between sampling units. The Bray– Curtis distance index was used to determine the dissimilarity in bird composition among sampling units (Legendre and Legendre 1998). Pearson’s correlation

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index was used to test the correlation between bird species abundance and richness, considering all bird groups. When variables were highly correlated (r ≥ 0.80), one of them was excluded from the analysis, since it would be redundant to analyse correlated variables. The same analysis was used to test for correlations among the independent variables (distance of pastures from natural habitats, number of trees and shrubs, tree height and canopy cover), and in the same way, any variables that were highly correlated (r ≥ 0.80) were excluded. Relationships between the dependent variables (species richness or abundance of each bird group, excluding migratory birds) and independent variables (distance of pastures from natural habitats, number of trees and shrubs, tree height and canopy cover) were tested using Generalised Linear Models (GLMs), with a Poisson error distribution for species richness and abundance. We tested the following hypotheses with different models: Null Model – there are no relationships between bird richness and/or abundance and any of the independent variables; Distance Model – bird species richness and/or abundance in pastures is explained only by the distance of a pasture from natural habitat; Vegetation Model – only vegetation structure (number of trees and shrubs, tree height and canopy cover) explains bird species richness and/or abundance in pastures; Vegetation + Distance Model – vegetation and distance from natural habitats together explain bird species richness and/or abundance in pastures. We used the Akaike Information Criterion corrected for small sample sizes (AICc) to select the models that best explain the variation in species richness and/or abundance of each bird group in pastures. The best model was the one that had the lowest AICc, but all models with ΔAICc ≤ 2 relative to the best model were considered equally plausible. The weight of each model (ωi), which determines the strength of the evidence, was also calculated (Burnham and Anderson 2002). The statistical relationship between bird composition in pastures (excluding migratory birds) and the independent variables was tested using Canonical Correspondence Analysis (CCA), since this method is robust and performs quite well even with skewed distributions (Palmer 1993; Ter Braak 1995). The explanatory power of the independent variables was tested with an ANOVA-like permutation test for CCA using 999 permutations (Legendre and Legendre 2012). Variations in the abundances of each bird species among pastures according to the independent variables were demonstrated by Direct Ordination, using only bird species that occurred in at least three sampling units. This cut-off was chosen to allow plotting of a manageable number of species by excluding species

(n = 30) of more sporadic occurrence. The ordination of samples and species was done by multidimensional scaling using a Bray–Curtis association matrix. All statistical analyses used in this study were performed with the software R (R Core Team 2013) using the ‘VEGAN’ package (Oksanen et al. 2009).

Results Nineteen forest and 49 semi-forest bird species were recorded in the study pastures (Table S1, supplementary material). The sampling units had a mean of 2.19 individuals (SD ± 3.20, min = 0, max = 19, n = 84) of 0.94 forest bird species (SD ± 1.18, min = 0, max = 5, n = 84), and 6.28 individuals (SD ± 4.89, min = 0, max = 20, n = 84) of 3.82 semi-forest bird species (SD ± 3.20, min = 0, max = 13, n = 84). The trophic groups of birds with the greatest species richness in the pastures were frugivores, with 15 species (six forest and nine semi-forest), insectivores, with 26 species (eight forest and 18 semi-forest), and insectivores-frugivores, with 21 species (six forest and 15 semi-forest) (Table S1, supplementary material). There was no spatial autocorrelation among samples (R = –0.0012, p = 0.68, n = 84), indicating that geographic distance among sampling units did not affect pasture bird communities. Species richness and abundance were correlated for all bird groups (all r > 0.80), and so only species richness was tested, since the variables correlated with abundance in the same way. Moreover, for our purposes, the relationship between the number of bird species and the independent variables in pastures is more important than the relationship with bird abundance. All independent variables were included in the analysis because no pair of variables showed values of r ≥ 0.80. The Vegetation Model best explained species richness of forest birds in pastures, with the number of trees and shrubs being the best predictor variable for these birds, with higher species richness in pastures with more trees and shrubs (Table 1). The Vegetation Model (ωi = 0.584) was also the best model for explaining species richness of semi-forest birds in pastures, but the Vegetation + Distance Model (ωi = 0.401) was plausible too (Table 1). The richness of forest frugivores in pastures was best explained by the Distance Model. Thus, species richness of forest frugivorous birds decreased as the distance between pastures and natural habitats increased (Table 1). The richness of semi-forest frugivorous birds was best explained by the Null Model (Table 1). Species richness of forest insectivores was best explained by the Vegetation (ωi = 0.435) and Vegetation + Distance (ωi = 0.431) models. The most important variable for these birds was the number of

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Table 1. Best and plausible models (in bold) and the main independent variable (in italic) which explain the bird richness in pastures Bird groups Forest birds

Semi-forest birds

Forest frugivorous birds

Semi-forest frugivorous birds

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Forest insectivorous birds

Semi-forest insectivorous birds

Forest insectivorous-frugivorous birds

Semi-forest insectivorous-frugivorous birds

Models Null Distance Vegetation + Distance Vegetation Number of trees and shrubs Null Distance Vegetation + Distance Vegetation Vegetation Null Vegetation + Distance Distance Distance of natural habitats Vegetation + Distance Vegetation Distance Null Distance Null Vegetation + Distance Vegetation Number of trees and shrubs Distance Null Vegetation + Distance Vegetation Tree height Distance + Vegetation Vegetation Distance Null Null Distance Vegetation + Distance Vegetation Number of trees and shrubs

AICc 233.8 232.0 230.3 228.3

ΔAIC 5.48 3.72 2.02 0

ω 0.039 0.095 0.256 0.610

390.5 384.8 378.1 377.3 97.8 97.7 96.3 92.6

13.15 7.48 0.75 0 5.21 5.07 3.73 0

0.001 0.014 0.401 0.584 0.056 0.060 0.119 0.765

211.1 209.1 205.3 204.2 107.1 105.0 102.1 102.0

6.87 4.93 1.16 0 5.05 2.95 0.02 0

0.019 0.051 0.334 0.596 0.035 0.099 0.431 0.435

262.7 260.8 259.0 256.9

5.72 3.88 2.07 0

0.037 0.092 0.228 0.643

156.3 155.1 153.2 152.6 222.2 216.3 208.8 207.7

3.75 2.49 0.60 0 14.5 8.63 1.10 0

0.070 0.132 0.339 0.459 0.000 0.008 0.363 0.628

t

p

2.26

0.02

−2.01

0.04

2.02

0.04

2.41

0.01

2.31

0.02

We tested whether the vegetation structure and distance from natural habitats explain the bird richness in pastures of RPPN Estância Mimosa, Bodoquena Mountains, western Brazil.

trees and shrubs, with greater richness in pastures with greater arboreal and shrubby cover (Table 1). The richness of semi-forest insectivorous birds was best explained by the Vegetation Model, with tree height being the most important variable, with greater richness in pastures with taller trees (Table 1). The richness of semi-forest insectivorous-frugivorous birds was best explained by the Vegetation (ωi = 0.628) and Vegetation + Distance (ωi = 0.363) models, with richness increasing in pastures with more trees and shrubs (Table 1). Finally, the Null Model best explained species richness of forest insectivorous-frugivorous birds in pastures (Table 1). The CCA and ANOVA-like permutation test found that bird species composition in EM pastures was also affected by vegetation structure and distance from natural habitats (F = 1.53; p ≤ 0.01). The four CCA axes explained 61.7% of the total variance in the bird composition in EM pastures (Table 2). The main independent variables on axis 1 (CCA1) were distance to natural habitats (with positive values) and number of

trees and shrubs (with negative values, just like the other vegetation structure variables). Axis 2 (CCA2) had distance of natural habitats as the main variable, while the vegetation structure variables were less important. Axes 3 and 4 (CCA3 and CCA4) had tree height and canopy cover as the most important variables (Table 2). Direct Ordination showed that some bird species were more abundant in pastures that were closer to Table 2. Results of Canonical Correspondence Analysis (CCA) for the relationship between composition and abundance of birds with the independent variables (in italic) in pastures CCA axes Eigenvalues Biplot scores for the independent variables Distance of natural habitats Number of trees and shrubs Tree height Canopy cover

CCA1 CCA2 CCA3 CCA4 30% 14.15% 9.8% 7.8% 0.60 −0.92 −0.55 −0.39

−0.74 −0.05 0.08 0.44

−0.27 0.21 −0.34 0.16 −0.60 −0.56 −0.75 0.27

We tested whether the vegetation structure and distance from natural habitats explain the composition and abundance of birds in pastures of RPPN Estância Mimosa, Bodoquena Mountains, western Brazil.

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natural habitats (Trogon curucui, Pteroglossus castanotis, Celeus lugubris, Pyrrhura devillei, Cacicus haemorrhous, Amazona amazonica, Dacnis cayana, Turdus leucomelas, Turdus rufiventris and Megarynchus pitangua) (Figure 1), while some were more abundant in pastures with more trees and shrubs (T. curucui, Cyanocorax chrysops, C. lugubris, Cyanocorax cyanomelas, Aburria cumanensis, P. devillei, A. amazonica, D. cayana, T. leucomelas and M. pitangua) (Figure 2), with taller trees (C. chrysops, T. curucui, C. cyanomelas, A. amazonica, M. pitangua, Veniliornis passerinus, Dryocopus lineatus and T. leucomelas) (Figure 3) and with greater canopy cover (C. lugubris, C. cyanomelas, A. amazonica and T. leucomelas) (Figure 4).

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Discussion Two hundred and forty-seven bird species have been recorded from the mosaic of forests, savannas and pastures of EM (Godoi et al. 2014). Among these, 106

species (43%) occurred in pastures (Godoi et al. 2016), of which 68 (64%) exhibited some degree of dependence on forest habitats (forest or semi-forest species). These data demonstrate that EM pastures were used by a great number of bird species of the region, including many forest species. Although anthropogenic pastures commonly possess lower bird species richness than surrounding natural habitats, they are still used by many species, indicating the importance of managing these areas for bird conservation (Harvey et al. 2006; Mendoza et al. 2014; Godoi et al. 2016). The results of the present study showed that vegetation structure and distance from natural habitats may affect the species richness, composition and abundance of forest and semi-forest birds that occur in pastures of the Bodoquena Mountains in the Cerrado domain of western Brazil. In particular, the abundance of trees and shrubs may affect forest birds, forest insectivorous birds and semi-forest insectivorous-frugivorous birds, while tree height may be important to semi-forest

Figure 1. Changes in bird abundance (black bars) and composition in pastures in relation to the distance to natural habitats (in metres), RPPN Estância Mimosa, Bodoquena Mountains, western Brazil.

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Figure 2. Changes in bird abundance (black bars) and composition in pastures in relation to the number of trees and shrubs, RPPN Estância Mimosa, Bodoquena Mountains, western Brazil.

insectivorous birds, and the distance from natural habitats seems to be important to forest frugivorous birds. These data are in accordance with other studies that showed vegetation structure may be important to the bird species richness, composition and abundance (Tews et al. 2004; Jayapal et al. 2009; Jankowski et al. 2012). In addition, birds of different trophic groups and with different habitat requirements may be affected in different ways by vegetation structure (Cueto and De Casenave 2000; Hasui et al. 2007; Ding et al. 2008; Laube et al. 2008; Jayapal et al. 2009; Jankowski et al. 2012). Forest birds, for example, had greater richness in pastures with more tree and shrub cover, as was found in other studies (Harvey et al. 2006; Laube et al. 2008; Mendoza et al. 2014). Some forest birds were more abundant in pastures with greater numbers of trees and shrubs, including insectivores (C. lugubris), frugivores (A. cumanensis and P. devillei) and insectivoresfrugivores (T. curucui, C. chrysops and C. cyanomelas).

Tree height was important in pastures, as was also found by Laube et al. (2008). In the pastures of EM, species richness of semi-forest insectivorous birds was greater in areas with taller trees, and many birds were most abundant in these areas (A. amazonica, C. chrysops, V. passerinus, M. pitangua and D. lineatus). Although canopy cover did not explain the richness of any of the bird groups, some bird species were most abundant in pastures with more canopy cover, such as C. lugubris, C. cyanomelas, A. amazonica and T. leucomelas. The importance of vegetation structure for birds in pastures could be because more trees and shrubs, as well as taller trees, offer more food resources and sites for foraging, nesting and perching (Saab and Petit 1992; Silva et al. 1996; Estrada et al. 1997; Fischer and Lindenmayer 2002; Luck and Daily 2003; Harvey et al. 2006). In addition, pastures with less tree cover may make birds more susceptible to predation (Estrada et al. 1997) and extreme weather (Wilson et al. 2005), which may explain the lower richness in these pastures.

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Figure 3. Changes in bird abundance (black bars) and composition in pastures in relation to tree height (in metres), RPPN Estância Mimosa, Bodoquena Mountains, western Brazil.

An important element for birds in pastures is the presence of fruiting trees, which can be used as a source of food for frugivorous birds that inhabit surrounding areas (Luck and Daily 2003; Eshiamwata et al. 2006), inciting their movement through these pastures. Increased mobility of frugivorous birds in pastures can increase the chance of seed dispersal from surrounding natural habitats, contributing to forest regeneration of anthropogenic areas (GalindoGonzalez et al. 2000; Martínez-Garza and GonzálezMontagut 2002), bringing benefits to the human economy by recovering degraded areas (Sekercioglu et al. 2004; Sekercioglu 2006). In the pastures of EM, for example, there are plant species that produce many fruits that attract birds, thereby making pastures more appealing for foraging. This is the case for capororoca (Rapanea guianensis, Myrsinaceae), a tree whose fruits are consumed by a great diversity of birds in the savannas and pastures of EM (M. N. Godoi pers. obs.), and belongs to a genus known to be important

to the diet of many bird species (Pineschi 1990; Francisco and Galetti 2001; Pascotto 2007). Another important factor that may affect bird species richness, composition and abundance in the EM pastures is pasture distance from natural habitats. Some forest (T. curucui, P. castanotis, C. lugubris, P. devillei and C. haemorrhous) and semi-forest (A. amazonica, D. cayana, T. leucomelas, T. rufiventris and M. pitangua) birds occurred only, or were most abundant, in pastures nearby to natural habitats. The proximity of forest patches seems to be an important factor for the occurrence of forest birds in pastures and the richness of these birds is usually higher in crops and pastures closer to natural habitats (Naidoo 2004; Laube et al. 2008). In EM, the forest frugivorous birds present in pastures seem to be greatly affected by the distance from natural habitats, which is in agreement with other studies that showed that there is lower species richness of these birds in crops and pastures farther from natural areas (Luck and Daily

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Figure 4. Changes in bird abundance (black bars) and composition in pastures in relation to canopy cover (in %), RPPN Estância Mimosa, Bodoquena Mountains, western Brazil.

2003; Laube et al. 2008). This finding may be due to the richness and abundance of fruits being greater in forests and savannas as compared to pastures (unpub. data), making the most distant pastures less attractive to frugivorous birds. The reduction in richness of forest frugivorous birds in pastures that are more distant from natural habitats can make seed deposition in these pastures less likely, slowing the process of natural regeneration, although this may be minimised by seed dispersal by semi-forest frugivorous birds. This may be the case in the EM pastures, where the richness of semi-forest frugivorous birds was not affected by distance from natural habitats, indicating that these species may be responsible for the majority of seed dispersal and regeneration in pastures farther from natural areas. The results of the present study show the importance of increasing vegetation heterogeneity in pastures and reducing their distance from natural habitats as management measures to make pastures more

accessible to bird species from surrounding natural environments. However, the conservation value of maintaining trees and shrubs in agricultural areas, and minimising the distance of crops and pastures from natural habitats, has been ignored (Naidoo 2004; Harvey et al. 2006; Laube et al. 2008). For example, in the Bodoquena Mountains, cattle ranching and more recently the expansion of traditional soybean plantations have established large areas without patches of native vegetation or even any trees and shrubs scattered within the pastures and crop fields. Overall, it is necessary to adopt several management practices to promote bird conservation in pastures and crop fields, such as maintaining and increasing the number of trees and shrubs, establishing live fences, promoting the regeneration of natural vegetation and preserving patches of native vegetation and corridors of riparian vegetation (Estrada et al. 1997; Petit et al. 1999; Wilson et al. 2005; Harvey et al. 2006). Adopting these management practices, instead of traditional production methods

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M. N. GODOI ET AL.

that promote the removal of entire areas of native vegetation, can help in the conservation of birds and other animal and plant groups in these pastures and crop areas.

Acknowledgements

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The authors are very grateful to Eduardo and Simone Coelho, the owners of ‘Reserva Particular do Patrimônio Natural (RPPN) Estância Mimosa (EM)’, for the opportunity and logistical support to carry out this study on their farm, and to EM staff for their help and hospitality during field collections. The authors also thank the reviewers of this article for their important contributions, and Hannah Lois Doerrier and Erik Wild for the English review. Mauricio Neves Godoi thanks the Universidade Federal de Mato Grosso do Sul and CAPES for financial support through a doctoral scholarship. Franco Leandro de Souza is funded by a research grant from CNPq (301071/2011-0).

ORCID Mauricio Neves Godoi 0979

http://orcid.org/0000-0002-9415-

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