Urban Ecosyst (2012) 15:111–131 DOI 10.1007/s11252-011-0195-2

Relation between green spaces and bird community structure in an urban area in Southeast Brazil Maria Cecília Barbosa de Toledo & Reginaldo José Donatelli & Getulio Teixeira Batista

Published online: 16 July 2011 # Springer Science+Business Media, LLC 2011

Abstract Increased urbanization typically leads to an increase in abundance of a few species and a reduction in bird species richness. Understanding the structure of biotic communities in urban areas will allow us to propose management techniques and to decrease conflicts between wild species and human beings. The objective of this study was to describe the structure of the bird community in an urban ecosystem. The study was carried out in the city of Taubaté in southeastern Brazil. Point-counts were established in areas with different levels of tree density ranging from urban green spaces to predominantly built-up areas. We looked for a correlation between the richness/abundance of birds and the size of the area surveyed, the number of houses, the number of tree species and the number of individual trees. The results of multiple regression showed that bird richness had a direct relationship with vegetation complexity. The abundance and diversity of tree species were better predictors of bird species than the number of houses and size of the area surveyed. We discuss implications of this study for conservation and management of bird diversity in urban areas, such as the need to increase green areas containing a large diversity of native plant species. Keywords Urban birds . Urban vegetation . Bird-habitat relationship . Brazil

M. C. B. de Toledo (*) Universidade de Taubaté, Instituto de Biociências, Laboratório de Ecologia, Av. Tiradentes, 500 Bom Conselho, CEP: 12010-180 Taubaté, SP, Brazil e-mail: [email protected] R. J. Donatelli Departamento de Ciências Biológicas, Universidade Estadual Paulista—UNESP, Bauru, SP, Brazil e-mail: [email protected] G. T. Batista Departamento de Ciências Agrárias, Universidade de Taubaté, Taubaté, SP, Brazil e-mail: [email protected]

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Introduction Most studies conducted in cities located in temperate regions of the world have attempted to address the effects of urbanization on species diversity and used birds to investigate the factors that influence the distribution, abundance and conservation status of urban avifauna (e.g. Catterall et al. 1989; Jokimäki and Suhonen 1993; Hostetler 1999; Fernández-Juricic 2000; MacGregor-Fors 2008; Rodewald and Shustack 2008; Álvarez and MacGregor-Fors 2009). Birds are especially useful because they are conspicuous, interact with several other organisms, and require a wide variety of habitats at different spatial scales (Bibby et al. 2000; MacGregor-Fors 2008). Studies carried out with birds have shown that urbanization can lead to species extinction due to replacement of the natural environment by built-up areas (Marzluff 2001; Jokimäki and Suhonen 1998). Chace and Walsh (2006) described some of the emergent patterns of bird community responses to the process of urbanization as follows: (1) a reduction in species richness, (2) an increase in bird biomass, and (3) selection for omnivorous, granivorous, and cavity nesting species. These patterns are the result of processes such as (1) changes in vegetation composition and structure (Emlen 1974; Catterall et al. 1989; Melles et al. 2003; MacGregor-Fors 2008); (2) fragmentation (Friesen et al. 1995; Fernández-Juricic and Jokimäki 2001; Fernández-Juricic 2004); (3) the introduction of exotic species (Mills et al. 1989; Khera et al. 2009); (4) human activities and human presence (Miller et al. 1998; Álvarez and MacGregor-Fors 2009); and (5) the availability of anthropogenic food (Mills et al. 1989; Jokimäki and Suhonen 1993; Piper and Catterall 2006). Nevertheless, studies of birds in tropical urban settings are limited (Marzluff 2001; Chace and Walsh 2006; MacGregor-Fors 2008) and investigations of the dynamics of neotropical bird communities in urban area are lacking. Perhaps this is because the complex patterns and processes related to the immense neotropical bird diversity are still beginning to be determined even for natural ecosystems, considered more important than urban settings. In Brazil, the general influence of urbanization is small when compared with agricultural development across the immense land territory. However, the opposite is true for southeastern Brazil where conversion of natural Atlantic Forest into managed systems and urban areas is steadily increasing. Works carried out in neotropical regions with the purpose of assessing bird responses to urbanization are emerging (Manhaes and LouresRibeiro 2005; Rodewald and Shustack 2008; López-Flores et al. 2009; Álvarez and MacGregor-Fors 2009; Garaffa et al. 2009), and this may yield yet unknown patterns and processes, contributing substantially to the ecological knowledge of urban birds. At the moment, general patterns have been observed in urban areas that are independent of the ecosystem in which the city is embedded (Clergeau et al. 2001). Thus, it is necessary to develop a fine scale assessment of the processes and patterns that are associated with the effects of urbanization in neotropical regions, especially regarding biological consequences which remain poorly explored (Clergeau et al. 2006). According to Marzluff (2005), bird species richness is reduced in areas with more than 60% of the surface dominated by built structures or with more than ten human residences per hectare. The opposite tendency is observed in areas that are covered by trees and bushes; the greater the number of trees and bushes, the higher the bird richness (Melles et al. 2003). At a fine vegetation scale, the vertical structure (Melles et al. 2003; Sandström et al. 2006), the floristic composition (Khera et al. 2009; Lin and Sodhi 2004; MacGregor-Fors 2008) and the area covered by vegetation (Daniels and Kirkpatrick 2006; Garaffa et al. 2009) are excellent predictors of bird species richness. Therefore, it is important that the relationships among these variables for bird conservation in neotropical regions be understood.

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The focus of this study was to generate knowledge about urban bird diversity, focusing on the status of bird richness and abundance in built-up areas and urban green spaces (public gardens and city parks) located in the SW Atlantic region of Brazil. In addition, the aim was to determine if habitat characteristics affect bird communities both in built-up areas and in urban green spaces and to determine if richness and abundance of birds that live in the city change along gradients from areas that are highly urbanized to urban green spaces. We predicted (1) that size of the green space should be positively correlated with richness and abundance of birds, (2) that size of blocks and number of houses in built-up areas should be negatively correlated with bird species richness and positively correlated with bird abundance, and (3) that tree richness and tree abundance in both built-up and urban green spaces should be positively correlated with richness as well as abundance of birds.

Methods Study area This study was carried out in the city of Taubaté, State of São Paulo, Brazil (45° 33′ 20″ W and 23° 01′ 35″ S; 550 ma.s.l.). The human population size is about 300,000 inhabitants (IBGE-Instituto Brasileiro de Geografia e Estatística 2001). The municipality includes a total area of 626 km² and an urban area of 106 km², of which about 32.5 km² correspond to a more densely populated nucleus (Fig. 1). The downtown core of Taubaté City is the oldest and most highly urbanized. A commercial center is surrounded by residential blocks with varying and randomly distributed built-up/green space patches. The peripheral area comprises new residential zones, mostly housing projects, together with industrial zones. The outskirts, located between the urban periphery and the rural area, presents remnant patches of secondary Atlantic Rainforest, savanna (“cerrado”) and semi-deciduous seasonal forest (Ferreira 2007). Agricultural activities, mainly rice crops, eucalyptus reforestation and pasture, characterize the rural area. Choice of sampling areas Analyses of urban areas were based on satellite images using three multispectral bands with 2.40 m resolution fusioned with a panchromatic band with 0.6 m of spatial resolution (Fig. 1). A GIS-based map of urban Taubaté was developed using SPRING v. 3.5.1 (Câmara et al. 1996). We produced three maps: (1) map of green spaces and built-up areas (Fig. 2); (2) map of blocks according to housing density (map 2 was made by coupling map 1 to a file containing polygonized blocks), in which the size of the sampling area was calculated and high housing density (>60% impervious area), medium housing density (30–60% impervious area) and low housing density (<30% impervious area) were selected; and (3) map containing public parks and gardens. The final product was a map in raster format with blocks classified according to the percentage of built-up areas and green spaces. Green spaces By green spaces we meant all public parks, public gardens, and greenways (avenues and streets) used by human inhabitants for walks, recreation, relaxing or other purposes. Green space size varied (mean=0.7±0.8 ha). Ten green spaces (sampling area) were selected for field work, and all of them contained a mixture of natural and

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Fig. 1 Southeast of Brazil, São Paulo State (black points correspond to important areas to bird conservation, modified of Bencke et al. 2006), and Taubaté City (red point) in the Image (A=green space; B=built-up areas)

exotic vegetation. They were similar in landscaping, age, vehicle and pedestrian flow (Fig. 3a, b, and c). Forest fragments were not included in the sample. To characterize green spaces, trees and bushes over 2 m high were counted and identified. Built-up areas We considered built-up blocks those with more than 10% impervious areas including residences, commercial buildings, apartment buildings, paved and concrete surfaces. From the map of blocks showing the percentage of built-up areas and green spaces, 30 blocks were selected—10 blocks for each housing density (Fig. 3e, f and g). After selecting sampling areas, visits were made to the sites to choose the most similar blocks regarding construction type. Industrial areas and blocks containing more than one apartment building were excluded from the sample. Blocks varied according to size (8.3±3.9 ha). A state government’s program in the 70’s established an extensive plantation of only one species (Caesalpinia pluviosa), and few individuals of other species were maintained. Thus, the vegetation in built-up areas and green spaces is poor in shrubs and herbaceous diversity. Another important factor is that all green spaces showed similar human activities, such as the flow of vehicles, bicycles and people. In this case, the major difference was between days of the week and weekends. For this reason, surveys were conducted on weekends. In particular, (1) number of tree species, (2) number of trees (including trees/large bushes >2 m), and (3) size

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Fig. 2 Map of Taubaté city separating the areas (1) blocks with high housing density (black), (2) blocks with medium housing density (gray), and (3) blocks with low housing density (white)

of green spaces were evaluated. We also evaluated (1) number of houses by block, (2) size of blocks (3) tree richness, and (4) tree abundance. Bird survey This study was carried out over 1 year (from May 2002 to May 2003). Observations were made in the morning from 05h00 to 11h00 on weekends only. A few pilot surveys identified that there was no significant difference in detection of bird species, and this interval of time allowed the observer to move among the sampling areas. The method of point-counts (Bibby et al. 2000) was used to quantify the community of birds in built-up areas and green spaces. A count was made once a month at each green space and block; specifically, 40 areas were sampled 12 times. Four point-counts (one per side) were positioned within each built-up area. In green spaces, the number of count stations differed by size of area; in the largest green spaces, up to four points were used and in the smallest ones only one point was used. Observation times were held constant for all sampling areas because one point by green space and built-up area was drawn and visited at different hours, with the purpose of avoiding bias due to point numbers and time of day factors. The spacing between point count sites varied from 200 m to 500 m, as this is the minimum distance recommended to avoid double counting (Bibby et al. 2000). Bird surveys were conducted by the same observers on clear and calm days. At each point count site, all individual bird species seen and/or heard were recorded during

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Fig. 3 Illustrations of sampling units showing in the top blocks with low housing densities (a), with medium housing densities (b), and with high housing densities (c). In the bottom, areas with green spaces, including PF Park (d), JK1 garden (e), and PQu Park (f)

10 min periods, including the flying species. Aquatic birds were ignored. Bird nomenclature follows the Records of International Ornithological Committee list (Gill and Donsker 2010). Data analysis We determined the differences among bird community structures by comparing the steepness of the bird community evenness/dominance slopes using a bird species rank per abundance plot approach (Magurran 1988). To evaluate statistical differences among slopes, we performed ANCOVA and the Newman-Keuls post hoc range test. Since bird abundance

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values differed greatly in each class of built-up areas and green spaces, we used abundance transformed (Ln) values. Bird species were classified into trophic groups. To group the birds we used primary feeding resource categorized into six dietary categories: insectivore (i), frugivore (f), nectarivore (n), grass seeds eater (g), carnivore (c), and omnivore (o), based on descriptions by Sick (1997) and based on personal observation in the field. To test if different classes of urban gradients affected richness values, we used ANOVA one-way test and Newman-Keuls post hoc test on the total number of species along the year and mean abundance for the year. For each level of urbanization, we computed species richness (Sobs Mao Tau ±95% CI) using EstimateS (Colwell 2005). We computed the mean number of individuals and standard errors (x±SE). We used the Shapiro-Wilk test to check for normality, and variables with non-normal distributions were either log(x +1), −1*log(x), or arcsin(x) transformed to make suitable normal distributions. Another analysis was carried out with native species only found in green spaces with the purpose of isolating the effect of Common Pigeon (Columba livia) and House Sparrow (Passer domesticus) in abundance values. The abundance of Common Pigeon and House Sparrow was analyzed separately in built-up areas. Richness may respond to more than one environmental variable because interactions among variables may occur. To assess the effect that habitat attributes have on bird species richness and individual abundance, we used stepwise multiple regression analysis. The objective of this analysis was to determine the contribution of each variable and the best diversity models. Dependent variables used were total annual richness and mean annual abundance. Independent variables used for blocks were (1) size of the area surveyed (ha), (2) number of trees, (3) number of houses, and (4) number of tree species; for green spaces (1) size of the area surveyed (ha), (2) number of trees, and (3) number of tree species. When two or more variables contributed to a significant correlation (R>0.4; p<0.05), they were maintained in the analysis even if the p-value of the independent variable was little significant. Three multiple regressions were run on built-up areas (richness, abundance of birds, and exotic birds) and three on green spaces (richness, abundance and native species).

Results A total of 65 tree species were recorded. The most common species in the green spaces were False Brazilwood (Caesalpinia pluviosa) with 26% of abundance, Yellow Trumpet Tree (Tabebuia ochracea) and Pink Trumpet Tree (Tabebuia impeginosa), which together accounted for 20% of abundance, and Figs Tree (Ficus sp.) with 8.78% of abundance (Appendix 1). Vegetation in built-up areas was characterized based on trees and bushes counted and identified in areas of public access around the blocks. A total of 18 tree species were recorded, and the most abundant were False Brazilwood (Caesalpinia pluviosa) with 35.7%, followed by Orchid Tree (Bauhinia aculeate) with 12%, and Golden Cane Palm (Dypsis lutescens) with 10% of abundance (Appendix 2). Sixty-four species belonging to 26 families were observed (Table 1). The most abundant species (≥80% of the sampled community) were House Sparrow (Passer domesticus), Common Pigeon (Columba livia), Blue-and-white Swallow (Notiochelidon cyanoleuca), Ruddy Ground-Dove (Columbina talpacoti), and Sayaca Tanager (Thraupis sayaca). Those found in over 90% of the sites were House Sparrow, Blue-and-white Swallow, Ruddy Ground-Dove, Sayaca Tanager (Thraupis sayaca), Bananaquit (Coereba

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Table 1 Values obtained for the average number of individual per species (NM), frequency of occurrence (FO), trophic groups (GT), habitat (H), and occurrence class in the urban gradient: (1) HHD (blocks with high density housing), (2) MHD (blocks with medium density housing), and (3) LHD (blocks with low density housing) Family / Species

N

FO

GT H

Class HHD MHD LHD Green

Accipitridae Buteo magnirostris (Roadside Hawk)

0.07 0.0013 c

Ae

*

Columba livia (Common Pigeon)

9.59 0.1695 o

So

Columba picazuro (Picazuro Pigeon)

0.04 0.0126 g

Ar

Zenaida auriculata (Eared Dove)

0.3

0.0067 o

So

Columbina talpacoti (Ruddy Ground-Dove)

7.62 0.1350 o

So

0.03 0.0021 f

Ar

0.07 0.0013 i

Ar

0.02 0.0013 c

So

Eupetomena macroura (Swallow-tailed Hummingbird)

0.76 0.0135 n

Su/ar *

Thalurania glaucopis (Violet-capped Woodnymph)

0.26 0.0046 n

Su/ar

Amazilia lactea (Sapphire-spangled Emerald)

0.07 0.0021 n

Su/ar *

Amazilia fimbriata (Glittering-throated Emerald)

0.26 0.0029 n

Su/ar

Chlorostilbon aureoventris (Glittering-bellied Emerald)

0.23 0.0046 n

Su/ar *

0.16 0.0013 i

ar

0.11 0.0050 i

so

0.33 0.0038 i

ar

0.28 0.0013 i

ar

Columbidae *

*

*

* *

*

* *

*

*

*

*

Psittacidae Forpus xanthopterygius (Blue-winged Parrotlet) Cuculidae Crotophaga ani (Smooth-billed Ani)

*

*

*

Strigidae Athene cunicularia (Burrowing Owl)

*

Trochilidae *

*

* *

*

* *

* *

Picidae Picumnus cirratus (White-barred Piculet)

*

*

*

Furnariidae Furnarius rufus (Rufous Hornero)

*

Tyrannidae Camptostoma obsoletum (Southern Beardless-Tyrannulet) Todirostrum cinerium (Common Tody-Flycatcher)

*

*

* *

Elaeniidae Phyllomyias griseocapilla (Gray-capped Tyrannulet)

0.04 0.0008 i

ar

Suiriri suiriri (Suiriri Flycatcher)

0.16 0.0055 i

ae

* *

*

*

Elaenia flavogaster (Yellow-bellied Elaenia)

0.04 0.0029 i

ar

*

*

*

Elaenia obscura (Highland Elaenia)

0.02 0.0008 i

ar

Serpophaga subcristata (White-crested Tyrannulet)

0.04 0.0008 i

ar

*

*

*

Fluvicolinae Myiophobus fasciatus (Bran-colored Flycatcher)

0.04 0.0021 i

Fluvicola nengeta (Masked Water Tyrant)

0.02 0.0008 i

so

*

Machetornis rixosa (Cattle Tyrant)

0.07 0.0059 i

so

* * *

*

*

*

Tyranninae Myiarchus tyrannulus (Brown-crested Flycatcher)

0.3

0.0038 i

ae

Pitangus sulphuratus (Great Kiskadee)

0.35 0.0240 o

ar

* *

*

*

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Table 1 (continued) Family / Species

N

FO

GT H

Class HHD MHD LHD Green

Myiozetetes similis (Social Flycatcher)

0.04 0.0004 i

ae

Tyrannus melancholicus (Tropical Kingbird)

0.21 0.0038 i

so

7.97 0.1409 i

ae

*

* *

*

*

Hirundinidae Notiochelidon cyanoleuca (Blue-and-white Swallow) Stelgidopteryx ruficollis

*

0.0050

*

*

*

*

*

*

*

*

Troglodytidae Troglodytes aedon (House-Wren)

1.07 0.0189 i

su

*

Turdidae Turdus amaurochalinus (Creamy-bellied Thrush)

0.11 0.0097 f

So/ar

Turdus rufiventris (Rufous-bellied Thrush)

0.04 0.0008 f

so

*

* *

Turdus flavipes (Yellow-legged Thrush)

0.14 0.0013 f

ar

*

0.09 0.0034 f

ar

1.71 0.0303 n

ar/su

Mimidae Mimus saturninus (Chalk-browed Mockingbird)

*

*

*

*

*

Coerebidae Coereba flaveola (Bananaquit)

*

Thraupidae Tangara cayana (Burnished-buff Tanager)

0.11 0.0021 f

ar

Thraupis sayaca (Sayaca Tanager)

4.09 0.0723 f

ar

*

*

*

*

Thraupis palmarum (Palm Tanager)

0.14 0.0093 f

ar

*

*

*

Dacnis cayana (Swallow Tanager)

0.52 0.0021 f

ar

*

Emberizidae Zonothrincha capensis (Rufous-collared Sparrow)

0.11 0.0004 o

so/su

*

Sporophila caerulescens (Double-collared Seedeater)

0.57 0.0004 g

su

*

0.19 0.0063 f

ar

0.54 0.0122 g

su so/ar

Fringillidae Euphonia chlorotica (Purple-throated Euphonia)

*

*

*

*

*

*

*

*

*

Astrildidae Estrilda astrild (Common Waxbill) Passeridae Passer domesticus (House Sparrow)

14.9

0.2641 o

*

GT = carnivorous (c), insectivorous (i), frugivorous (f), nectarivorous (n), granivorous (g), or omnivorous (o); H = arboreal (ar), aerial (ae), tussocks or understory (su), and ground (so)

flaveola), House-Wren (Troglodytes aedon), and Swallow-tailed Hummingbird (Eupetomena macroura). Only three species, Common Pigeon, Common Waxbill (Estrilda astrild), and House Sparrow, were exotic and recorded over the entire urban area. Among the most abundant and most widely distributed species, occurrences that were significantly different between built-up areas and green spaces included: Common Pigeon (F=169.5; p<0.001); Ruddy Ground-Dove (F=14.76; p<0.001); Bananaquit (F = 21.71; p = 0.001); House Sparrow (F = 13.09; p < 0.001); House-Wren (F = 6.4; p<0.01). Common Pigeon, Ruddy Ground-Dove, House Sparrow, and House-Wren were more common in built-up areas, and Bananaquit was very common in green spaces.

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Trophic composition Bird species represented by six trophic groups were recorded. The numbers of bird species in each group were as follows: omnivore (n=6), insectivore (n=20), nectarivore (n=6), granivore (n=3), frugivore (n=10), and carnivore (n=2). A bird was considered carnivore only if it was a top predator and if it feeds on small vertebrates and large invertebrates. A group that drew our attention was the nectarivorous species (n=6), in relation to the number of species present in the urban area. Insectivores were the dominant group in Taubaté, and omnivores were the dominant group in areas with high housing density. Community structure The structure of bird communities was recorded considering both the urban gradient of housing density and the different vegetation covers. Slopes from the species rank/ abundance plots were statistically different among categories (ANCOVA: F3,204 =5.18, P=0.025), showing higher evenness and lower dominance in green spaces (Fig. 4). Such differences were significant between green spaces and high housing density blocks (p<0.000), green spaces and medium housing density blocks (p<0.01), and green spaces and low housing density blocks (p < 0.05). The green space areas had a more even distribution of bird abundances and higher species richness than the three types of built-up areas examined. Bird richness values increased from built-up areas with higher housing density to green spaces (Fig. 5a). When we compared species richness, significant differences among the four groups assessed were observed (F=21.99; p<0.000). Bird richness in green spaces (47±3.1) was significantly higher than in areas with high and medium housing density (p<0.05). Richness in both high housing density areas (26.5±2.6) and medium housing density areas (36.3±2.8) were lower but not significantly different. Likewise, in low housing density areas (42.5±2.9) it was not significantly different than in green spaces. Abundance was different in the four types of areas assessed (F=3.35; p<0.029). The highest abundance value was observed in high housing density blocks (849±6.1), followed by green spaces (637±6.6), medium density blocks (456±3.2) and low housing density blocks (304±3.4). Only low housing density blocks differed

Fig. 4 Relation between bird species rank and abundance for the urban gradient vegetation studies: (HHD) blocks with high housing density, (MHD) blocks with medium housing density, (LHD) blocks with low housing density and (GS) green spaces

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Fig. 5 Richness and abundance values of species bird in blocks of different high density. In the top, (a) all species are plotted, and in the bottom, (b) the more abundant species (Common Pigeon and House Sparrow) were withdrawn from the analysis

significantly from high housing density ones (p<0.05). When abundance values were analyzed without the two exotic and more abundant species (Common Pigeon and House Sparrow), there was a relationship with the urbanized gradient (Fig. 5b). Abundance values decreased from built-up areas with higher housing density (mean=532±3.7) to green spaces (mean=105±5.6). Relation with habitat attributes Habitat attributes differed for both blocks and for green spaces (Tables 2 and 3). Multiple regressions revealed that bird species richness values in Taubaté city were significantly and positively related to the richness of trees in both built-up areas and green spaces (Tables 2a and 3a). Conversely, the abundance of exotic birds in built-up areas and bird richness in green spaces were negatively related to tree abundance (Tables 2c and 3a). Total bird abundance in built-up areas showed a negative relationship with size of the area, number of houses (Table 2b), and with tree abundance in the green spaces (Table 3b). In green spaces, bird abundance was positively related to tree species richness. Additionally, in green spaces the abundance of native species was shown to be positively related to richness and abundance of trees (Table 3a).

Discussion and conclusions Non-native species such as Common Pigeon and House Sparrow were more dominant in the urban landscape. However, native species such as Ruddy Ground-Dove, Scaled Pigeon, Eared Dove, Swallow-tailed Hummingbird, Great Kiskadee, Blue-and-White Swallow,

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Table 2 Relationship of the habitat attributes with the richness and abundance of the birds in built-up areas. Bird richness exhibited a significant and positive relation with tree richness (a) and a negative pattern in relation to the area size; bird abundance was inversely related to number of houses and area size (b). When considering only exotic species (c) the relation was positive with tree abundance and negative with number of houses General model (R=0.98; F4,25 =403.3; P<0.0001) Beta

S.E.

t

p

(a) Richness Intercept Tree richness Area (ha)

1.0277 −0.630

0.0445 0.0289

0.5188

0.6105

23.065 −2.1759

<0.0001 0.0439

General model (R=0.68; F4,23 =6.23; P=0.011) Beta

S.E.

t

p

(b) Total abundance Intercept

10.172

<0.0001

House numbers

−0.3892

0.1928

−2.0187

0.0550

Area (ha)

−0.5083

0.2330

−2.1815

0.0486

General model (R=0.62; F2,25 =5.33; P=0.016) Beta S.E. t

p

(c) Exotic abundance Intercept

1.0668

0.3009

Tree abundance

4.6244

1.6787

2.7548

0.013532

House numbers

−2.0424

0.8347

−2.4468

0.025577

Bananaquit, and Sayaca Tanager were easily observed in Taubaté City. House Sparrows were abundant in all areas but were more common in parks, together with Common Pigeon, where they had food available and shelter. Our results showed strong evidence suggesting that covered areas with different levels of trees or buildings affect the bird community. Indeed, where buildings were prevalent, the bird community was dominated by few species. This pattern was supported by the records of high abundance and low number of species in built-up areas, and high number of species and low abundance in green spaces, showing a gradient in response to the quantity and richness of tree species and amount of impervious surface or built-up habitat. However, the community structure analysis suggested two sets of statistically recognized groups formed by (1) high and medium density housing blocks that were poor in bird species and (2) low housing density blocks and green spaces that were rich in bird species. The inverse pattern was recorded for bird abundance, that is, a decreased abundance with increasing area occupied by vegetation. Our results showed that these patterns can be, in part, explained by the relation between quantity and quality of trees. Bird species considered exclusively urban (Common Pigeon and House Sparrow) showed the highest number of individuals all over the city. A similar pattern is found in other cities in different countries (Fernández-Juricic 2000 (Spain); Melles et al. 2003 (Canada); Jokimäki and Kaisanlahti-Jokimäki 2003 (Finland); Daniels and Kirkpatrick 2006 (Australia); Khera et al. 2009 (India); Álvarez and MacGregor-Fors 2009 (Mexico); Garaffa et al. 2009 (Argentina). The omnivore species were the most dominant in all sampled areas, and insectivores were the trophic group with the highest number of species. Like other works conducted in neotropical regions such as Mexico (Álvarez and

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Table 3 Relationship of the habitat attributes with bird richness and abundance in green space. The richness and abundance of trees showed an important relation to the richness (a) and abundance (b) of birds. These factors are consistent with the analysis of the native species, (c) in which richness and abundance of trees were important to bird community structure General model (R=0.47; F3,10 =5.21; P<0.04) Beta

S.E.

t

p

(a) Richness Intercept

11.291

Tree richness

0.6604 −0.078

Tree abundance Area (ha)

1.5607

<0.000

0.078

2.9826

0.00137

0.005

−2.4779

0.0326

0.051

1.3363

0.2110

General model (R=0.72; F3,10 =19.4; P=0.002) Beta S.E. t

p

(b) Total abundance Intercept

6.8721

<0.0001

Tree richness

35.5016

2.110

6.2262

<0.0001

Tree abundance

−2.1538

4.927

−3.6460

0.0002

General model (R=0.70; F3,10 =14.01; P=0.001) Beta

S.E.

(c) Native species abundance Intercept Tree richness Tree abundance

t

p

0.7220

0.4841

14.7035

0.002

4.0148

0.0017

0.3965

0.315

3.6053

0.0036

MacGregor-Fors 2009) and Argentina (Leveau and Leveau 2004), insectivores were a predominant group in urban areas. A relevant aspect of urban areas is the abundance of herbivorous arthropods (Shochat et al. 2004). Faeth et al. (2005) refer to some groups of arthropods that are highly abundant in urban areas, such as generalist ground arthropods, plant-feeding arthropods, generalist pollinating and jumping spiders, and this factor may account for the predominance of insectivorous species in the area surveyed. Abundance and richness of nectarivorous species were interesting in areas with high housing density and were similar to the results observed by Hodgson et al. (2007), where the shortage of food is apparently large. People living in residential areas often have artificial bird feeders with nectar, fruits, and seeds. On several occasions, it was possible to see feeders in public green spaces, private gardens and houses, and apartment balconies. Altogether, this means that the food supply in residential areas can be good (Daniels and Kirkpatrick 2006). According to Clergeau et al. (2006), it is very difficult to make generalizations about trophic groups because of the presence of artificial feeding that can change the density and bird composition of assemblages. Native and exotic woody species such as Tabebuia spp., Chorisia speciosa, Bauhinia spp., and Erythrina speciosa were abundant in parks and streets of Taubaté city and are very attractive to hummingbirds (Toledo and Donatelli 2010). This suggests that green spaces with a wider spectrum of food resources (different kinds of fruits and flowers) offer an opportunity to many other species of arthropods and nectarivorous birds. According to different degrees of urbanization or vegetation, the distribution of bird species and abundance differed. We found that in green spaces, the bird community showed

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higher evenness and lower dominance of species in opposition to high housing density areas where the number of bird species decreased and abundance increased. Thus, our results suggest that the urbanization gradient affects the evenness and dominance of the bird community in a linear and negative manner. This pattern was similar to other works conducted in urban areas showing that the number of species declines with increasing urbanization and that the remaining group of species is dominated by highly abundant species (e.g., Emlen 1974; Melles et al. 2003; Garaffa et al. 2009; Álvarez and MacGregorFors 2009). The decrease in species richness in built-up areas can be explained by (1) limited size of lots and irregular occupation in areas with high housing density that leads to a reduction in the amount of vegetation, mainly tree species; (2) the poor diversity of native tree species planted on streets and avenues by the local administration; and (3) some pedestrians who damage the young plants and seedlings. In contrast, there is an expected increase in bird richness in blocks with lower housing density because (1) the majority of front and back yards are present in residences, and (2) many tree species and bushes are cultivated, mostly with flower and fruit species (both exotic and native). The yard is an important aspect for bird species conservation because it can substantially influence bird species composition (Daniels and Kirkpatrick 2006). The main problem in green spaces in Taubaté is the removal of understory plants and replacement of native bushes and trees by non-native species. In Brazilian cities, the natural environment is profoundly changed as an effect of urbanization, and Taubaté is no exception to the rule. Nowadays, the vegetation layout of Brazilian cities preserves little or almost none of the natural environment, making the urban landscape totally different from the original one (Kirchner et al. 1990). A good example of this change in urban green spaces is the predominance of the False Brazilianwood, which has an incidence of 50% to 70% in some cities of the State of São Paulo (Souza et al. 1990; Winters et al. 1992). Therefore, areas with 60% of tree cover are important to bird richness in cities like Taubaté. Multiple regression models for built-up areas evidenced the importance of tree diversity in maintaining bird richness. Considering the total abundance of birds in built-up areas, the number of houses and the size of blocks had a reverse effect. In other words, the higher the rate of urbanization, the lower the abundance of birds, mainly native species. The size of blocks is a result of irregular or badly planned land occupation, in which large blocks have many houses on small lots, especially in housing projects. This pattern has been widely observed in others studies (Leveau and Leveau 2004; Lin and Sodhi 2004; Melles et al. 2003; Khera et al. 2009). When only non-native species (Common Pigeon and House Sparrow) were analyzed in built-up areas, results showed a negative effect of tree abundance. This result confirms the hypothesis that intensively urbanized areas contribute to an increase in exotic bird species. In studies of urban gradients, similar results have been observed by Blair (1996), Clergeau et al. (2006), and van Rensburg et al. (2009). Multiple regression models for green spaces showed a different trend compared to builtup areas that were especially associated with floristic composition. Tree species richness was strongly related to bird richness and total bird abundance. Despite the little contribution to the general regression model, the number of trees was not positively correlated with total bird richness and abundance. On the other hand, when only native bird species were analyzed, both richness and abundance of trees contributed to a better structured community regarding abundance and richness of species. It is worth comparing the effect of abundance of trees both in green spaces (Table 2) and built-up areas (Table 3) on total abundance of birds and abundance of native species, the abundance of trees favoring native species and disfavoring non-native species populations.

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Results similar to those found in this study have been recorded in a city with temperate climate in the South of Brazil where the effect of tree density was positively related to native bird species composition, whereas population density was inversely related to bird diversity (Fontana et al. 2011). It is, therefore, clear that cities located in different climatic regions show similar effects as a result of little vegetation in the urban area. We expected that the size of the area surveyed would have had greater and significant contribution to the bird community present in green spaces as observed in other studies (Gavareski 1976; Garaffa et al. 2009; Khera et al. 2009). This may result from the characteristics of the vegetation in the area surveyed for, although these green spaces vary in size, the vegetation they contain is man-made and shows no relation between number of species and size of area as found in native forests. Habitat measures such as size of the area surveyed, number of trees, percentage cover of tree canopy, density of bushes, predominance of native plants and tree richness are good predictors of bird species in urban areas (Lancaster and Rees 1979; Green et al. 1989; Catterall et al. 1989; Day 1995; Jokimäki 1999; Melles et al. 2003; FernándezJuricic 2004). In this study, the number of trees showed great variation among the sampled areas, and much of this variation explained the presence or absence of bird species. Native bird diversity is more likely to be responsive to variations in the amount and type of vegetation (Day 1995; van Heezik et al. 2008; Khera et al. 2009). In this context, Bowman and Marzluff (2001) argued that cities may support a larger number of species compared to surrounding rural areas because the urban environment contains a mosaic of habitats and micro-environments such as gardens, lawns, orchards, lakes, walls, and hedges, among innumerable other habitats that may favor some species to live in urban areas. The present study was carried out in a Brazilian city embedded in the Atlantic forest ecosystem that has high diversity and endemism of bird species. The results are important to understand the effects of urbanization in this biogeographic region and confirm that some patterns reported previously in other countries and continents also apply to Taubaté City. Reflecting global trends, the southeast of Brazil is in an extensive process of urbanization. Consequently, the negative effects on bird diversity tend to increase. Urban management and planning activities based on floristic composition, structure, and development of green spaces can be manipulated to favor the bird community (Jokimäki 1999; Daniels and Kirkpatrick 2006; Álvarez and MacGregor-Fors 2009). Therefore, based on our results and field observation, we suggest that urban planning focus on the following: (1) improving the quality and complexity of floristic composition in public green spaces including streets, avenues and roads; (2) establishing environmental education projects to create an incentive for inhabitants to care for gardens, yards, and parks – both public and private; (3) increasing the connection between small green spaces by corridors aiming to generate an urban green network; and (4) implementing long-term monitoring programs using birds as bioindicators, including volunteers to create discussion groups for management actions. These recommendations aim to improve environmental quality for all species, including human beings.

Acknowledgements The authors are thankful to Maria Célia Villac for her support and advice. We also thank two anonymous reviewers who greatly improved the manuscript. Finally, we thank Martha Villac and Alberto Bezerril for the English proofreading.

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Appendix 1

Table 4 List of tree and woody shrub species, abundance, and relative abundance by greenspace samples. The names were revised according to Missouri Botanical Garden. 28 Jul 2010
Family

Individual numbers

Relative abundance (%)

Fabacea Moraceae Bignoniaceae Bignoniaceae†* Melastomataceae†* Arecaceae†* Fabacea Fabacea† Bignoniaceae†* Lauraceae Cupressaceae Salicaceae Strelitziaceae Myrtaceae Caryocaceaea† Myrtaceae Lauraceae Verbenaceae† Salicaceae Muntingiaceae Apocynaceae† Myrtaceae† Moraceae Rosceae Rosceae† Fabacea† Fabacea† Euphorbiaceae† Malvaceae† Cupressaceae Fabacea†* Urticaceae†* Polygonaceae† Fabacea Oleaceae Araucariaceae

65 43 35 32 14 12 10 9 5 5 4 4 4 4 3 2 2 2 2 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

23.7 15.7 12.7 11.7 5.1 4.4 3.6 3.3 1.8 1.8 1.5 1.5 1.5 1.5 1.1 0.7 0.7 0.7 0.7 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4 0.4

Fabacea† Arecaceae†* Araucariaceae†

16 11 7

16.7 11.5 7.3

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127

Table 4 (continued) Species

Family

Individual numbers

Tabebuia ochracea Cycas circinalis Euterpe oleracea Tabebuia impentigionosa Tibouchina granulosa Genipa americana Ceiba speciosa Delonix regia Malpighia glabra Roystonea oleracea Tabebuia alba Terminalia catappa Eugenia uniflora Filicium decipiens n.i. Callitris preissii Cecropia hololeuca Ficus sp. Ficus auriculata Maclura tinctoria Psidium guajava Syzygium aromaticum Syzygium jambos Tamarindus indica RN Psrk Mangifera indica Malvaviscus arboreus Hibiscus rosa-sinensis Mimosa bimucronata n.i.01 Cecropia hololeuca Psidium guayava Tabebuia alba Bougainvillea glabra Inga edulis Hymenaea stilbocarpa Codiaeum variegatum n.i.02 PQu Park Caesalpinia pluviosa Yucca guatemalensis Syagrus romanzoffiana PBC Park Senna multijuga Eugenia uniflora

Bignoniaceae† Cycadaceae Arecaceae Bignoniaceae Melastomataceae†* Rubiaceae†* Malvaceae†* Fabacea Malpighiaceae† Arecaceae† Bignoniaceae†* Cambretaceae Myrtaceae†* Spindaceae

6 5 5 5 5 4 3 3 3 3 3 3 2 2 2 1 1 1 1 1 1 1 1 1

Cupressaceae Urticaceae†* Moraceae Moraceae Moraceae†* Myrtaceae†* Myrtaceae Myrtaceae Fabacea Anacardiaceae Malvaceae Malvaceae Fabacea†*

Relative abundance (%) 6.3 5.2 5.2 5.2 5.2 4.2 3.1 3.1 3.1 3.1 3.1 3.1 2.1 2.1 2.1 1 1 1 1 1 1 1 1 1

11 10 7 6 3 3 2 2 2 1 1 1 1

22 20 14 12 6 6 4 4 4 2 2 2 2

Fabacea† Asparagaceae Arecaceae†*

18 4 3

72 16 12

Fabacea†* Myrtaceae†*

8 2

50 12.5

Urticaceae†* Myrtaceae†* Bignoniaceae†* Nyctaginaceae†* Fabacea Fabacea†* Euphorbiaceae

128

Urban Ecosyst (2012) 15:111–131

Table 4 (continued) Species

Family

Individual numbers

Relative abundance (%)

Terminalia catappa Syzygium jambos Persea americana Tabebuia alba Bauhinia purpurea PF Park Ficus guaranitica Cupressus lusitanica Bauhinia aculeata Delonix regia Yucca guatemalensis Ficus sp. Syagrus romanzoffiana Psidium guajava Caesalpinia pluviosa Tabebuia ochrcea Cinammomum sp. Maclura tinctoria Syzygium jambos JK1 Caesalpinia pluviosa Eugenia uniflora Joannesia princeps Ligustrum japonicum Yucca guatemalensis Tabebuia alba Dypsis lutescens Machaerium acutifolium JK2 Caesalpinia pluviosa Tabebuia impetiginosa Tabebuia alba Ligustrum japonicum Tecoma stans Persea americana Thuja sp. Mangifera indica Ficus benjamina Schinus terebinthifolius Malvaviscus arboreus Xylopia aromatica Eriobotrya japonica Jacaranda mimosifolia

Cambretaceae Myrtaceae Lauraceae Bignoniaceae†* Fabacea

2 1 1 1 1

12.5 6.2 6.2 6.2 6.2

Moraceae†* Cupressaceae Fabacea† Fabacea Asparagaceae Moraceae Arecaceae†* Myrtaceae Fabacea† Bignoniaceae† Lauraceae Moraceae†* Myrtaceae

15 14 7 5 4 3 2 2 2 2 2 2 1

24.6 23 11.5 8.2 6.6 4.9 3.3 3.3 3.3 3.3 3.3 3.3 1.6

Fabacea† Myrtaceae†* Euphorbiaceae†* Oleaceae Asparagaceae Bignoniaceae†* Arecaceae Fabacea†*

31 6 5 2 1 1 1 1

64.6 12.5 10.4 4.2 2.1 2.1 2.1 2.1

Fabacea† Bignoniaceae Bignoniaceae†* Oleaceae Bignoniaceae Lauraceae Cupressaceae Anacardiaceae Moraceae Anacardiaceae†* Malvaceae Annonaceae† Rosceae Bignoniaceae†

54 34 25 16 8 5 5 3 2 1 1 1 1 1

34.4 21.7 15.9 10.2 5.1 3.2 3.2 1.9 1.3 0.6 0.6 0.6 0.6 0.6

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129

Table 4 (continued) Species PD Park Caesalpinia pluviosa Bauhinia variegata Syagrus romanzoffiana DEp Park Caesalpinia pluviosa Syagrus romanzoffiana † *

Family

Individual numbers

Relative abundance (%)

Fabacea† Fabacea Arecaceae†*

4 2 1

57.1 28.5 14.21

Fabacea† Arecaceae†*

4 1

80 20

exotic species to Brazil exotic especies to study area

Appendix 2

Table 5 List of tree and woody shrub species, abundance, and relative abundance by build-up samples. The names were revised according to Missouri Botanical Garden. 28 Jul 2010
Family

Individual numbers

Caesalpinia pluviosa

Fabacea

92

35.7

Bauhinia aculeata

Fabacea†

32

12.4

Dypsis lutescens

Arecaceae

26

10.1

Bauhinia variegata

Fabacea

17

6.6

Syagrus romanzoffiana

Arecaceae†*

14

5.4

Lagerstroemia indica

Lythraceae

14

5.4

Tabebuia alba Malvaviscus arboreus

Bignoniaceae†* Malvaceae

14 6

5.4 2.3

Ligustrum japonicum

Oleaceae

6

2.3

Tecoma stans

Bignoniaceae

6

2.3

Hibiscus rosa-sinensis

Malvaceae

5

1.9

Caesalpinea pulcherrina

Fabaceae†

4

1.6

Erythrina speciosa

Fabacea†*

5

1.9

Grevillea banksii

Protzaceae

5

1.9

Justicia brandegeana Chorisia speciosa

Acanthaceae† Malvaceae

4 3

1.6 1.2

Prunus campanulata

Rosaceae

1

0.4

Mangifera indica

Anacardiaceae

3

1.2

Terminalia catappa

Cambretaceae

1

Total † *

exotic species to Brazil exotic especies to study area

226

Relative abundance (%)

0.4 100,0

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