Urban Ecosystems (2021) 24:375–390

https://doi.org/10.1007/s11252-020-01045-8

Vegetation structure drives taxonomic diversity and functional traits

of birds in urban private native forest fragments
Lucas Andrei Campos-Silva 1 & Augusto João Piratelli 2

Accepted: 27 July 2020 / Published online: 30 July 2020

# Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract
Many studies in urban landscapes have revealed that vegetation structure influences the taxonomic diversity and traits of birds
and drives greater bird richness in greenspaces. However, most of these studies have been carried out mainly in public spaces.
Private lands represent large components of cityscapes worldwide, and so understanding the role they play in the maintenance of
biodiversity, and how vegetation traits drive the ecological attributes of birds, remain poorly known. Here we identified local
factors of vegetation related to the bird fauna of urban private native forest fragments in Sorocaba, state of São Paulo, Brazil, with
a focus on their ecological attributes. We predicted that increased vegetation structure would select birds that depend on forest
environments and the resources they support. We sampled 13 vegetation traits in 28 private urban native forests to evaluate the
relationship between vegetation structure and taxonomic diversity and functional traits of birds. Confirming our prediction,
vegetation structure shaped the ecological attributes of birds, with five vegetation traits driving bird taxonomic diversity and
functional traits, of which the number of standing dead trees was related to more bird ecological attributes. Vegetation structure in
urban private native forest fragments may increase habitats and resources, thus supporting habitat- and feeding-specialist species.
Our results provide insights for public policies aimed at management and maintaining vegetation structures that benefit bird fauna
(e.g. number of standing dead trees, tree richness, canopy cover), in support of the ecological functions they perform in urban
landscapes.

Keywords Urban greenspaces . Bird functional traits . Neotropical cityscapes . Resources

Introduction Ibáñez 2017), has changed the spatiotemporal patterns of nat-

Urbanization is a global anthropogenic process that converts
natural areas into landscapes with human presence and its
artifacts (Marzluff 2001). Modern cities have grown very
quickly and complexly around the world, leading to irregular
spatial patterns (Ramalho and Hobbs 2012). This unbalanced
and often disordered growth (MacGregor-Fors and Escobar-
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s11252-020-01045-8) contains supplementary
material, which is available to authorized users.
* Lucas Andrei Campos-Silva
andrei.10@hotmail.com
* Augusto João Piratelli
piratelli@ufscar.br
1
Programa de Pós-Graduação em Ecologia e Recursos Naturais,
Universidade Federal de São Carlos, São Carlos, SP, Brasil
2
Departamento de Ciências Ambientais, CCTS, Universidade Federal
de São Carlos, Sorocaba, SP, Brasil
ural ecosystems and biological communities, often resulting in
the loss of species and the downgrading of ecosystem func-
tions and services (Kremen and Ostfeld 2005; McKinney
2006; Cruz et al. 2013; Sacco et al. 2013; Myczko et al.
2014, but see Blair 1996; Leveau 2019).
Urban areas shelter nearly 20% of the world’s bird species
(Aronson et al. 2014), mostly in greenspaces (Ortega-Álvarez
and MacGregor-Fors 2009). These species respond in differ-
ent ways to urbanization, either by avoiding, tolerating or
exploiting (Blair 1996; Marzluff 2001; Caula et al. 2008;
Shochat et al. 2010; Evans et al. 2015; Rayner et al. 2015;
Seress and Liker 2015; González-Lagos and Quesada 2017;
Piratelli et al. 2017; Murgui and Hedblom 2017). The occur-
rence of birds in urban settlements can be influenced by both
the regional (e.g. original species pool; Lizée et al. 2011) and
local effects (e.g. the distance from water bodies, noise level,
impervious surface, human population density, and
greenspaces; Sol et al. 2014; Pena et al. 2017; Barbosa et al.
2020; and references therein). Urban greenspaces are com-
posed of patches of native and exotic species that contrast in
376
structure and vary in size and vegetation characteristics
throughout a mosaic of private and public lands (Taylor and
Hochuli 2017). Urban greenspaces, such as parks, squares,
gardens, and reserves, are usually created mainly for recrea-
tional purposes, but they are also manageable and can repre-
sent refuges for biodiversity (MacGregor-Fors et al. 2016).
Research carried out mainly in such greenspaces has
highlighted bird-habitat relationships within cities. They have
emphasized local vegetation structure (i.e. ecological
characteristics of plant communities that may provide habitats
and resources; e.g. richness and abundance of tree and shrubs,
presence of understory and canopy; Shipley 2009; Rutten et al.
2015) as a key ecological component for habitat heterogeneity
because it shapes the composition of urban avifauna (Marzluff
2001; de Toledo et al. 2012; Barth et al. 2015; Beninde et al.
2015; Huang et al. 2015; MacGregor-Fors et al. 2016; Lepczyk
et al. 2017). Losses of green areas and the reduction of native
forest remnants drives losses in local environmental structure
and heterogeneity, which leads to dramatic declines in diversity
and richness of target species, such as habitat and food
specialists (Chace and Walsh 2006; Partecke et al. 2006;
Evans et al. 2009; Strohbach et al. 2013; Barth et al. 2015).
Reduction of natural structures, such as tree and shrub species
and the number of standing dead trees, decreases habitat
heterogeneity at the local level, which is negatively related to
bird assemblages (Carbó-Ramírez and Zuria 2011; Myczko
et al. 2014; Paker et al. 2014).
Most of this knowledge about bird-habitat relationships in
urban areas comes from studies in urban greenspaces, either
urban public greenspaces, such as gardens (Paker et al. 2014),
graveyards (Čanády and Mošanský 2017), parks (Zhou et al.
2012) and riparian areas (Pennington and Blair 2011;
Dallimer et al. 2012), or private gardens (Chamberlain et al.
2004; Cannon et al. 2005; Daniels and Kirkpatrick 2006; van
Heezik and Adams 2016). However, little is known about how
vegetation structure drives urban bird communities in private
urban native forests. This knowledge is central to understand-
ing the ecology of urban birds because private areas may
represent a large portion of this ecosystem (e.g. Loram et al.
2007; Davies et al. 2009), and can play an important role in
providing urban biodiversity, ecological functions and ecosys-
tem services (Daniels and Kirkpatrick 2006; Davies et al.
2009; Goddard et al. 2010; van Heezik and Adams 2016).
Public areas do not impose access restrictions; however, pos-
session of them can be granted for limited periods of time, in
the public interest (Sorocaba 2019). Private areas are sites with
restricted access to people and/or vehicles, regulated by fed-
eral law and municipal acts (Brazil 2017).
High rates of urbanization have been reported within
Brazilian biodiversity hotspots, such as the Atlantic Forest
and Cerrado (Seto et al. 2013), and sites recognized as prior-
ities for conservation have already been recorded within pri-
vate urban settlements (de Mello et al. 2016). Understanding
Urban Ecosyst (2021) 24:375–390
patterns of species composition and identifying the habitat
structures that shape bird composition within urban ecosys-
tems, not only in public but also in private native forests, is
one of the greatest challenges for sustainable city planning and
conservation of natural resources (Fontana et al. 2011;
Aronson et al. 2014; Ferenc et al. 2014).
One type of private area in the urban context that may
shelter some important urban greenspaces, such as native for-
ests, are the private gated communities. This new type of land
use is sprawling in the Neotropics, and especially in Brazil.
The first Brazilian gated community was implemented in the
1970 s in the state of São Paulo. The number of gated com-
munities in the country as a whole increased during the 1990 s,
with these new components of urban landscapes being gener-
ally located outside of central areas (Freitas 2008; Barros
2012; Silva et al. 2015). In Brazil they are defined as walled
or fenced residential areas governed and approved by
Brazilian Federal Law 6,766/79 (Brazil 1979). They also have
guardhouses and/or gates operated by private security agents
that control access to dwellings and other spaces. All gated
communities in Brazil must preserve at least 20% of their area
as “green areas” destined for leisure and human well-being
while promoting the conservation of local biodiversity
(Resolução SMA-031, São Paulo 2009). The role that this
type of private urban area plays in maintaining biodiversity
is unknown.
The present study aimed to identify vegetation characteris-
tics related to bird fauna in private urban forests, focusing on
their ecological attributes. We hypothesized that vegetation
structure drives the taxonomic diversity and functional traits
of birds. We predicted that increased vegetation structure in
private forested areas selects birds that depend on forest envi-
ronments and resources (i.e., have functional traits linked with
habitat and food resource specializations). The data provided
here will contribute to filling a knowledge gap regarding ur-
ban avifauna and thus support public policies aimed at biodi-
versity conservation in cityscapes. To our knowledge, this is
the first study on birds in urban private native forest fragments
in the Neotropics.
Methods
Study areas
The study was carried out in the city of Sorocaba, southeastern
Brazil (23°30’5.65"S, 47°27’9.46"W; 632 m a.s.l., Fig. 1a, b).
Sorocaba encompasses about 450 km² and has ~ 670,000 in-
habitants, for a density of over one-thousand inhabitants per
square kilometer. The annual population growth rate is 1.75%.
Most inhabitants (98%) live in urban areas (IBGE 2019),
which represent 66% of the city, with the remaining native
vegetation consisting of patches of Atlantic Forest and
Urban Ecosyst (2021) 24:375–390
Cerrado, mostly (~ 60%) smaller than one hectare (de Mello
et al. 2016). The climate is subtropical with dry winters (tem-
peratures below 18ºC) and hot summers (over 22ºC), an aver-
age annual precipitation of 1,311 mm and an average annual
temperature of 22.1ºC (Alvares et al. 2013). The dry season
extends from April to September and the rainy season from
October to March (INMET 2020).
We studied a total of 28 private urban native forests. The
types of vegetation found in these urban forests are the
Atlantic Forest (Seasonal Semideciduous Forest) and the
Cerrado (Cerradão). These urban private native forest frag-
ments were located among 17 gated communities (~ 60% of
the local gated communities) within a maximum distance of
8 km from the city center (Fig. 1c, d). The areas vary greatly in
size and are mostly fragmented and small, ranging from 0.1 to
5.45 hectares. They have different levels of human interfer-
ence, and thus vary in their local characteristics (Fig. 1e,
Online Resource 1, Online Resource 2). Some areas had a
dominance of individual trees of just a few species, mostly
typical of early-succession and anthropogenic areas, with high
seed production and rapid growth (e.g. Piptadenia
gonoacantha). These areas also had trees planted (e.g.
Fig. 1 Location of the study area at five distinct scales. a Location of
Brazil in South America; b location of Sorocaba in the state of São Paulo;
c boundary of the city of Sorocaba showing urban area (light gray) and
377
Croton urucurana) in the beginning and throughout the estab-
lishment of the gated communities, which are found mainly at
the edges of the green areas. Some of these areas also had their
understory cleared or depleted by managers for aesthetic, rec-
reational, and public safety reasons (Online Resource 1b),
which is a common practice in urban areas (Heyman 2010).
Bird surveys
Bird censuses were performed, and environmental variables
were measured, from September 2016 to September 2017.
Bird communities were sampled by performing 10-minute
fixed-point counts (20-meters radius) in the first four hours
of the day beginning at dawn. Aerial insectivores, shorebirds,
waterfowl, raptors and nocturnal and crepuscular species were
not included because fixed point counts are not effective at
detecting these birds (Bibby et al. 2000; Pennington and Blair
2011). All individuals recorded perching, nesting, feeding or
flying beneath the canopy (or in the understory) were consid-
ered. Birds that had less than four records were excluded from
the analyses.
gated communities (dark grey) sampled with the point counts (red dots);
d examples of urban forest fragments (in green) of three gated
communities (dark gray); e interior of studied urban forests fragments
378
A total of 46 points, distributed among fragments accord-
ing to size (“one to six” per fragment, Online Resource 2),
were sampled. The points were separated from each other by
at least 200 m to reduce overestimation of species abundance
(Vielliard et al. 2010). Each point was georeferenced. Point-
counts were considered sample units. Two samplings were
performed at each point, with one in the rainy season and
one in the dry season, for a total of 92 sample units. Bird
taxonomy followed Version 4 of the Handbook of the Birds
of the World and BirdLife International (2019).
Vegetation characteristics
Thirteen vegetation characteristics were measured to evaluate
the effects of habitat structure. Measurements were made in
10 × 10 m plots in the center of each point on the same days of
bird censuses in the rainy season (Table 1; Online Resource
3). We assumed, based on previous evidence, that these veg-
etation characteristics are related to bird fauna (McElhinny
et al. 2005; Strohbach et al. 2013; Ferenc et al. 2014;
Beninde et al. 2015; Chang and Lee 2016).
Data analysis – Taxonomic diversity and functional
traits
Margalef’s richness (D’), Shannon-Wiener’s diversity
(H), and Pielou’s evenness (J’) indexes, and abundance
(number of contacts per point) were calculated to describe
bird taxonomic diversity across the studied sites. The
Margalef’s index is calculated including the number of
species and the total amount of individuals in a sample,
and the range has no limit (Gamito 2010). The Shannon-
Wiener diversity index mixes both richness (the number
of species) and equitability and can range from 0 to 5
(relative frequency, Bitetti 2000). Pielou’s evenness mea-
sures the deviation from an even distribution of individ-
uals in a community and can range from 0 to 1 (Ricotta
and Avena 2003). Birds were grouped according to five
functional traits (i.e., ecological attributes closely related
to a species functional role; Díaz and Cabido 2001;
Lavorel and Garnier 2002; Naeem and Wright 2003;
Suding et al. 2008; Fontana et al. 2011; Díaz et al.
2013): feeding group (plant/seed consumers, invertivores,
frugivores/nectarivores, omnivores); foraging stratum
(ground, understory, mid-high, canopy, mixed); forest de-
pendence (high, intermediate, low); cavity dependence for
nesting (non-dependent, secondary cavity nesters-ex-
ploiters, constructors) and body mass. Feeding groups
and foraging stratum were based on Wilman et al.
(2014) and personal observations, while forest depen-
dence followed Parker et al. (1996), Harris and Pimm
(2008), Becker et al. (2013), Vale et al. (2018) and
Urban Ecosyst (2021) 24:375–390
personal observations (Online Resource 4). Bird species
were grouped into five body-mass classes following
Dunning (2008): 0–49 g, 50–99 g, 100–149 g, 150–
199 g, ≥ 200 g.
Variance inflation factors (VIF) were calculated for the
vegetation variables to avoid collinearity (Zuur et al. 2010).
These factors measure the fraction by which the variance of
the regression coefficient is overestimated by the occurrence
of other explanatory variables (Boccard et al. 2011). This was
done using the function “vifstep” of the ‘usdm’ package
(Naimi et al. 2014) in R software (R Core Team 2015).
Vegetation variables with values greater than three were ex-
cluded from the analysis (Resource Online 5, 6, Zuur et al.
2010).
To analyze the relationships between vegetation and
taxonomic and functional diversity, we separated the tests
by univariate and multivariate responses. For the univari-
ate responses (richness, diversity, and evenness), we use
the generalized linear model (GLM) with a Gaussian dis-
tribution of errors. To do this we use the function “glm”
of the “stats” package in R software (R Core Team 2015).
Before that, we tested the spatial autocorrelation of these
indexes using the function “Moran.I” from the package
“ape” (Paradis and Schliep 2019) in the software R (R
Core Team 2015), and found no spatial autocorrelation
(p = 0.200, p = 0.870 and p = 0.921 to richness, evenness
and diversity, respectively). The GLM analyses were per-
formed by standardizing the vegetation variables to the
same dimension or scale.
Redundancy analyses (RDA) were performed to ana-
lyze the relationships between multivariate responses
(abundances of species by groups of forest dependence,
and the traits) and vegetation variables. Redundancy anal-
yses were performed after spatial autocorrelation tests for
both the response variables and the explanatories vari-
ables of vegetation. When an autocorrelation was identi-
fied, the factor was added as a covariate in the RDA to
remove its effect. For this, a binary connectivity matrix
(spatial neighborhood, object of class nb) was first built
using the coordinates of the point-counts. This matrix was
then used to build a spatial weighting matrix (SWM,
Gabriel type, object of class listw). These two steps were
performed using the functions “listw.candidates” and
“listw.explore()”of the “adespatial” package (Dray et al.
2020), which is a wrapper to package “spdep” (Bivand
and Wong 2018; Dray et al. 2020). The spatial weighting
matrix was used to build Moran’s Eigenvector Maps
(MEM), which are orthogonal vectors that maximizing
spatial autocorrelation, measured by Moran’s coefficient
(Dray et al. 2006). The spatial predictors were used as
covariates in the final RDA analysis. The spatial correla-
tion for each response and vegetation characteristics (pre-
dictable variables) were tested and significant MEMs
Urban Ecosyst (2021) 24:375–390 379

Table 1 Vegetation variables and

the methods of their measurement
in private urban greenspaces in
Sorocaba, São Paulo, Brazil.
Measurement methods based on
Ferreira and Laurance (1997),
Melo et al. (2007), Gschwantner
et al. (2009), Hunter et al. (2013)
and Galetti et al. (2018)
Variable Acronym Method of measurement
Tree morphospecies richness Tr.ric Count of the total number of tree morphospecies, with a tree
being a species of perennial plant that typically forms a
single self-supporting main stem which has a definite crown
Tree individuals Tr.ind Count of the total number of individual trees, regardless of
species.
Shrubs morphospecies richness Sh.ric Count of the total number of shrub morphospecies, with a
shrub being a species of perennial plant that does not form a
single main stem nor a defined crown (Gschwantner et al.
2009).
Shrub individuals Sh.ind Count of the total number of individual shrubs, regardless of
species.
Number of standing dead trees Dea.tr Count of total number of standing dead trees.
Litter cover Lit.co Measurements were obtained using a square of PVC tubing
Grass cover Gra.co (0.5 × 0.5 m) subdivided into four sub-squares
(0.25 × 0.25 m). The square was thrown randomly onto the
soil five times for each count point (center and four ex-
tremities of the 10 × 10 m area). Percentage of each variable
was visually estimated and total average percentage of the
area calculated.
Litter height Lit.he Litter height was measured in each sub-square of the square of
PVC tubing during the measurements of litter and grass
percentages by inserting a ruler and recording the measure-
ment when the ruler reached the soil.
Canopy cover C.co A spherical concave densiometer was used to measure the
percentage of squares occupied by light that passed through
the canopy, assuming lower luminosity means higher the
canopy cover. The densiometer was set at the breast height
(1.50 m), and five measurements were made, one at the
center and one at each of the four corners of the 10 × 10 m
area, and the average calculated.
Highest tree Hig.tr Height from the base to the canopy of the highest tree was
estimated using a digital tape.
Canopy height Can.he Visual estimate of the height of the tallest trees
Diameter at breast height M.dbh Stems of individual trees with diameter at breast height (DBH)
of the trees greater than 10 cm were measured using a tape-measure. All
stems were measured for multi-stem plants with at least one
stem of DBH greater than 10 cm. An average (M.dbh) was
calculated for each count point.
Standard error of the diameter at Std. Calculation of the standard error of diameter at breast height of
breast height of the trees error.- the trees for each count point.
dbh

were selected. For this, the function “moranNP.randtest”
of the package “adespatial” was used (Dray et al. 2020),
which allows describing whether there is a positive and/or
negative spatial correlation with the respective variable. If
there was a significant value for the index (number of
permutations = 1000), a further analysis was made by the
function “mem.select” of the “adespatial” package (Dray
et al. 2020). This function allows the identification of the
significant MEMs of the variable. For vegetation vari-
ables, “method = “MIR”” was used as the argument in
this function, while for multivariate responses “method =
“FWD"” was used. The argument “method = “MIR” was
used because it is the best choice to control spatial auto-
correlation in the model residuals (Bauman et al. 2018).
The argument “MEM.autocor = c(“positive / or nega-
tive”)” was also used in this function, specifying “posi-
tive” or “negative” to refer to which types of MEMs test-
ed significantly and should be selected based on the re-
sults of the previous function (“moranNP.randtest”). To
avoid the inflation of MEMs in the RDA analysis, only
one covariate with the same name was chosen for joining
all these MEMs selected from responses and vegetation
variables (see Online Resource 7 to check the results of
the spatial autocorrelation and the MEMs selected as
380
covariates in the RDA analysis). Fragment size for each
point-count was also added as a covariate in the RDA
models to remove possible relationships between frag-
ment size and the response variables.
The RDA analysis was performed by standardizing the
vegetation variables to the same dimension or scale be-
cause RDA is a linear method. Species abundance was
evaluated for groups of forest dependency to reduce the
risk of making a Type 1 error by increasing the number of
responses. Redundancy analysis is a multiple linear re-
gression followed by principal component analysis
(PCA) performed through the adjusted values table, in
which the matrix of the response variable (e.g. matrix of
species composition) is explained by a matrix of predic-
tive variables (Boccard et al. 2011). The double criterion
was used for the selection of explanatory variables to
avoid overestimating the number of explanatory variables
(Type 1 error; Blanchet et al. 2008). The selection crite-
rion used presents functions for the selection of the best
explanatory variables (i.e., the variables that explain most
of the variance; Boccard et al. 2011). For this, we used
the function “ordistep” of the “vegan” package (Oksanen
et al. 2019) in R software (R Core Team, 2015). This
function tests the significance of the F statistic, together
with all the explanatory variables, by permutation tests
(10,000 permutations), selecting the most significant ex-
planatory variables (based on p values). In the case of a
tie, the variable with the lower Akaike Information
Criterion (AIC) value was used. The process continues
until no more significant variables can enter the model.
Only “Scaling 2” was used for the graphical display of the
RDAs, such that the angle between descriptors in the
biplot reflects their correlation (Boccard et al. 2011).
A table with information on bird species presence in each
gated community (Online Resource 8), was also built to help
understand the distribution of species abundances in every
urban forest bird community.
Results
Taxonomic diversity
A total of 36 bird species were recorded, representing 15
families and six orders (Table 2, Online Resource 9). Five
variables were related to both birds’ taxonomic diversity
and functional traits. The variables that most positively and
negatively drove these bird components were number of
standing dead trees and tree individuals, respectively (re-
sults summarized in Fig. 2). Bird richness was related pos-
itively with number of standing dead trees (R2adj. partial =
0.200; t = 3.300; p = 0.002; Fig. 3a) and negatively with
tree individuals (R 2 adj. partial = 0.160; t = − 3.233; p =
Urban Ecosyst (2021) 24:375–390
0.002; Fig. 3b). Bird diversity was related positively with
number of standing dead trees (R2adj. partial = 0.140; t =
3.000; p = 0.005; Fig. 3c) and negatively with tree individ-
uals (R2adj. partial = 0.173; t = − 3.111; p = 0.004; Fig. 3d).
None of the vegetation variables were related to bird
evenness.
Tree richness and canopy cover drove abundance of low
forest-dependent birds, explaining 7.3% of the variance (R²adj
= 0.073, F = 2.662, p = 0.017). The first and second axes of
the RDA explained 84% and 16% of the variance, respective-
ly (Fig. 4). The species most positively related to these vari-
ables were Great Kiskadee (Pitangus sulphuratus), White-
eyed Parakeet (Psittacara leucophthalmus) and Tropical
Kingbird (Tyrannus melancholicus) (scores of the RDA1: -
0.460, -0.293, -0.130, respectively). The species most nega-
tively related to these variables were House Wren
(Troglodytes aedon), Ruddy Ground-dove (Columbina
talpacoti), Blue-black Grassquit (Volatinia jacarina) and
Eared Dove (Zenaida auriculata) (species scores of the
RDA1: 0.825, 0.300, 0.145 and 0.110, respectively). None
of the vegetation variables drove the abundance of species
with high and intermediate forest dependency (F = 1.910,
p = 0.110 and F = 1.15, p = 0.200, respectively).
Functional traits
Tree richness and individuals and the number of standing dead
trees were related to the number of species in each feeding
group and explained 10.1% of the total variance (R²adj =
0.101, F = 2.622, p = 0.015). The first and second axes ex-
plained 80% and 18% of the variance, respectively. Tree rich-
ness and the number of standing dead trees positively drove all
feeding groups, while tree individuals negatively drove all of
them (biplot of the vegetation variables: tree richness, -0.370;
number of standing dead trees, -0.368; tree individuals, 0.452;
species scores of the feeding groups of the RDA 1:
invertivores, -1.280; frugivores/nectarivores,-0.611; omni-
vores, -0.080 and plant/seed consumers, -0.190; Fig. 5).
Grass cover shaped the species richness of each forest de-
pendence group and was responsible for 7.2% of the total
variance (R²adj = 0.072, F = 4.300, p = 0.041). The first axis
of the RDA explained 100% of the variance. Grass cover
(biplot scores RDA1 = 0.927) positively drove the number
of low-forest-dependence species, and negatively drove the
number of high- and intermediate-forest dependence species
(species scores = 0.565, -0.090 and − 1.52, respectively,
Fig. 6).
The number of standing dead trees, canopy cover and tree
individuals drove the number of species of each cavity-
dependence group and were responsible for 19.4% of the total
Urban Ecosyst (2021) 24:375–390 381

Table 2 Birds species registered in the studied private urban greenspaces in Sorocaba, São Paulo, Brazil. Forest dependence: low- (L), intermediate- (I)
and high- (H). Cavity dependence: constructor, exploiter, and ND (non-dependent). Frequency of occurrence (FO); abundance (total contacts - TC)

Common name Scientific name Feeding group Foraging Forest Cavity Body FO TC
stratum dependence dependence mass (%)

Picazuro Pigeon Patagioenas picazuro Plant/Seed Mixed I ND ≥ 200 g 58.70 42

White-tipped Dove Leptotila verreauxi Plant/Seed Ground I ND 100–149 g 10.87 5
Eared Dove Zenaida auriculata Plant/Seed Mixed L ND 100–149 g 8.70 5
Ruddy Ground-dove Columbina talpacoti Plant/Seed Ground L ND 0–49 g 13.04 8
Planalto Hermit Phaethornis pretrei Frugivore/Nectarivore Understory I ND 0–49 g 13.04 6
Swallow-tailed Hummingbird Eupetomena macroura Frugivore/Nectarivore Mixed I ND 0–49 g 15.22 9
Common Squirrel-cuckoo Piaya cayana Invertivore Canopy I ND 100–149 g 6.52 3
Ochre-collared Piculet Picumnus temminckii Invertivore Understory H Constructor 0–49 g 8.70 4
Green-barred Woodpecker Colaptes melanochloros Invertivore Mixed I Constructor 100–149 g 13.04 5
Lineated Woodpecker Dryocopus lineatus Invertivore Mixed I Constructor 150–199 g 6.52 3
Blue-winged Parrotlet Forpus xanthopterygius Omnivore Canopy I Constructor 0–49 g 8.70 15
White-eyed Parakeet Psittacara leucophthalmus Plant/Seed Mixed L Constructor 150–199 g 8.70 11
Variable Antshrike Thamnophilus Invertivore Understory H ND 0–49 g 8.70 7
caerulescens
Sooty-fronted Spinetail Synallaxis frontalis Invertivore Understory I ND 0–49 g 8.70 6
Common Tody-flycatcher Todirostrum cinereum Invertivore Mixed I ND 0–49 g 39.13 26
Southern Beardless Camptostoma obsoletum Invertivore Mixed I ND 0–49 g 30.43 16
Tyrannulet
Yellow-bellied Elaenia Elaenia flavogaster Omnivore Mixed I ND 0–49 g 8.70 5
White-crested Tyrannulet Serpophaga subcristata Invertivore Mixed I ND 0–49 g 15.22 7
Great Kiskadee Pitangus sulphuratus Omnivore Mixed L ND 50–99 g 58.70 39
Boat-billed Flycatcher Megarynchus pitangua Invertivore Mixed I ND 50–99 g 8.70 4
Northern Streaked Flycatcher Myiodynastes maculatus Omnivore Mid-high I Exploiter 0–49 g 17.39 12
Social Flycatcher Myiozetetes similis Omnivore Mixed I ND 0–49 g 8.70 4
Tropical Kingbird Tyrannus melancholicus Invertivore Mixed L ND 0–49 g 15.22 10
Short-crested Flycatcher Myiarchus ferox Omnivore Understory I ND 0–49 g 6.52 3
Rufous-browed Peppershrike Cyclarhis gujanensis Invertivore Mixed I ND 0–49 g 10.87 7
House Wren Troglodytes aedon Invertivore Ground L Exploiter 0–49 g 58.70 39
Pale-breasted Thrush Turdus leucomelas Invertivore Mixed I ND 50–99 g 56.52 65
Purple-throated Euphonia Euphonia chlorotica Frugivore/Nectarivore Canopy I ND 0–49 g 23.91 11
Variable Oriole Icterus pyrrhopterus Invertivore Mixed I ND 0–49 g 8.70 8
Stripe-crowned Warbler Basileuterus culicivorus Invertivore Understory H ND 0–49 g 21.74 16
Bananaquit Coereba flaveola Frugivore/Nectarivore Understory I ND 0–49 g 63.04 51
Blue-black Grassquit Volatinia jacarina Omnivore Ground L ND 0–49 g 6.52 3
Orange-headed Tanager Thlypopsis sordida Omnivore Mid-high H ND 0–49 g 8.70 5
Sayaca Tanager Tangara sayaca Omnivore Mixed I ND 0–49 g 82.61 87
Palm Tanager Tangara palmarum Frugivore/Nectarivore Canopy I ND 0–49 g 21.74 14
Burnished-buff Tanager Tangara cayana Frugivore/Nectarivore Mixed I ND 0–49 g 26.09 19

variance (R²adj = 0.194, F = 4.230, p = 0.010). The first and
second axes of the RDA explained 96% and 4% of the vari-
ance, respectively. Tree individuals (biplot scores RDA1 = -
0.480) was negatively related to exploiters, constructors, and
non-dependents. The number of standing dead trees and can-
opy cover (biplot scores RDA1 = 0.454, 0.400, respectively)
were positively related to the number of exploiters, construc-
tors, and non-dependent species (species scores = 0.040,
0.135 and 2.103 respectively; Fig. 7). Neither foraging stra-
tum (F = 4.130, p = 0.380) nor body mass (F = 1.204, p =
0.300) were influenced by the sampled variables.
Discussion
Confirming our hypothesis that vegetation structure drives the
taxonomic diversity and functional traits of birds, vegetation
382
Fig. 2 Summary of vegetation variables that drove taxonomic diversity
and functional traits of birds of urban forest fragments of 17 private gated
communities in Sorocaba, São Paulo, Brazil. a Vegetation variables that
structure was found to be a key factor shaping bird taxonomic
diversity and functional traits in private urban forests. Our data
also support the prediction that vegetation structure would be
positively related to aspects of native bird species that depend
on forest resources (Fig. 2). Insectivorous and omnivorous
birds prevailed, as has been reported several times for urban
areas (Chace and Walsh 2006; MacGregor-Fors 2008; Ortega-
Álvarez and MacGregor-Fors 2011; Domínguez-López and
Ortega-Álvarez 2014; Pena et al., 2017; Barbosa et al.
2020). On the other hand, the present results agree with other
studies developed in forested areas regarding the predomi-
nance of species with functional traits with some dependence
on forest resources, such as mixed and understory foraging
stratum and intermediate forest-dependence (e.g., riparian,
Domínguez-López and Ortega-Álvarez 2014; Batisteli et al.
2018; Maure et al. 2018). The urban greenspaces studied here
are forested (Online Resource 1a), which favors forest-
dwelling species that require specific resources in these urban
landscapes. The predominance of insectivores and omnivores
is a recurrent pattern in urban landscapes and occurs because
Urban Ecosyst (2021) 24:375–390
positively drove ecological attributes of birds and their effects; b
vegetation variables that negatively drove ecological attributes of birds
and their effects
urbanization acts as a filter at both local and regional scales.
Neotropical bird communities are home to highly-diverse
families of insectivorous and frugivorous-insectivorous spe-
cies like Tyrannidae, many species of which can tolerate urban
conditions and forage in different strata (e.g. on the ground).
The number of standing dead trees was the most im-
portant driver of bird composition in these urban private
native forest fragments, not only for taxonomic diversity
but also for the functional traits, mainly specialized traits.
However, few studies have discussed the importance of
the number of standing dead trees for birds in urban eco-
systems (Morrison and Chapman 2005; Chace and Walsh
2 0 0 6; L e r m a n e t a l. 2 0 1 4 ; E s c o b a r - I b áñ e z a n d
MacGregor-Fors 2017; Tomasevic and Marzluff 2017;
Smith and Minor 2019). The number of standing dead
trees, along with canopy cover, comprise key ecological
resources for increasing richness of all nesting groups,
regardless of their cavity dependence. This result was ex-
pected since canopy cover and number of standing dead
trees increase vegetation structure, and thus deliver a
Urban Ecosyst (2021) 24:375–390
Fig. 3 Best ranked univariate models, showing the relationship between
vegetation variables and response variables of birds from urban forest
fragments in 17 private gated communities in Sorocaba, São Paulo,
Brazil. a Relationship between number of standing dead trees and bird
greater range of resources for birds, such as habitats, feed-
ing resources, and nesting sites (McElhinny et al. 2005).
The number of standing dead trees was also central to the
richness and diversity indexes (Fig. 3a, c). The greatest
amounts of standing dead trees were in the most conserved
private native forests, which were mainly unmanaged areas.
These sites have more vegetation structure, which favors the
presence and abundance of specialized urban forest-dwelling
birds. Unmanaged urban private native forest fragments can
shelter specialist forest birds by offering key resources, such
as food and nesting sites (Jokimäki 1999). Therefore, the man-
agement of these areas may have distinct effects on bird spe-
cies due to their diverse ecological demands.
The results for cavity-dependent species deserve to be
highlighted. Constructors, such as woodpeckers, play an im-
portant ecological role by creating nesting sites that can be
used by secondary cavity-exploiters (Martin and Eadie 1999;
Sekercioglu 2006; Tomasevic and Marzluff 2017). We also
stress the relationship between canopy cover and the number
383
richness; b Relationship between tree individuals and bird richness;
c Relationship between number of standing dead trees and bird
diversity; d Relationship between tree individuals and bird diversity
of standing dead trees and this ecological function, which
supports cavity-constructors, thus promoting secondary cavity
nesters-exploiters (Fig. 7). Ecosystem engineers are recog-
nized as species that rapidly disappear from highly anthropo-
genic areas, mainly due to limitations of their central resources
(Morrison and Chapman 2005; Myczko et al. 2014;
Tomasevic and Marzluff 2017). The present results show the
need for maintaining these important resources in urban areas,
not only for the constructors themselves, but also for other
beneficiaries such as the secondary cavity nesters-exploiters.
Contrary to our expectations, tree individuals negatively
drove some aspects of taxonomic diversity, such as richness
and diversity (Fig. 3b, d). These unexpected findings may be
explained by the dominance of individuals of some tree spe-
cies linked to the initial stages of ecological succession. These
tree species are common in areas with lower canopy cover, as
they are generally rapid colonizers with fast-growth and large
seed production. These trees may not supply food resources
(e.g., fruits and flowers) or nesting sites to local birds, leading
384 Urban Ecosyst (2021) 24:375–390

Fig. 4 Redundancy analysis

triplot of abundance of species
with low forest-dependence by
two vegetation variables of urban
forest fragments in 17 private
gated communities in Sorocaba,
São Paulo, Brazil. Scaling 2

Fig. 5 Redundancy analysis

triplot of bird feeding groups by
three vegetation variables of
urban forest fragments in 17
private gated communities in
Sorocaba, São Paulo, Brazil.
Scaling 2
Urban Ecosyst (2021) 24:375–390 385

Fig. 6 Redundancy analysis

triplot of bird forest dependence
by one vegetation variable of
urban forest fragments in 17
private gated communities in
Sorocaba, São Paulo, Brazil.
Scaling 2

Fig. 7 Redundancy analysis

triplot of bird cavity dependence
by three vegetation variables of
urban forest fragments in 17
private gated communities in
Sorocaba, São Paulo, Brazil.
Scaling 2
386
to a reduction in specialized birds, such as forest-dependent
species. Thus, some sites with more individual trees were also
more anthropized and with lesser vegetation structure,
reflecting on the observed local pattern. Dominance and ho-
mogenization of tree species can be common in urban land-
scapes, which can negatively drive some components of the
bird fauna (McKinney 2006; Trentanovi et al. 2013). The
present data agree with this explanation, mainly concerning
some functional traits, such as feeding groups (Fig. 5). Tree
richness was a determinant for the presence of specialized
feeding groups, such as some frugivores/nectarivores and
invertivores (Fig. 5), yet tree individuals had negative effects
on all feeding groups. Frugivores, nectarivores, and
invertivores perform crucial ecological functions such as seed
dispersal, pollination, and population control of arthropods,
respectively (Sekercioglu 2006). Therefore, an increase in
the number of trees, when not linked to tree species diversity,
may compromise the performance of ecological functions by
birds due to the loss of functional traits. An increase in native
tree species richness may improve vegetation structure and
spatial heterogeneity, and thus provide a larger set of condi-
tions and resources for bird fauna (Ferenc et al. 2014; Chang
and Lee 2016).
We found that grass cover may have distinct effects on
species richness related to the level of forest dependence
(Fig. 6). As the sampled areas are remnants of native forests,
sites with high grass cover may benefit low forest-dependent
birds by increasing open spaces. On the other hand, they may
negatively be related to intermediate- and high-dependent spe-
cies, by decreasing central forest resources (e.g., tree richness,
number of standing dead trees, and the structure of understo-
ry). Indeed, we agree with previous findings that vegetation
structure influences the composition of urban bird communi-
ties (Croci et al. 2008b; Fontana et al. 2011; Ferenc et al. 2014;
Schütz and Schulze 2015).
Distinct patterns were also detected for the abundance of
low forest-dependent species related to vegetation structure.
Fruit- and arthropod-eating birds, like Great Kiskadee, White-
eyed Parakeet and Tropical Kingbird, were positively driven
by tree richness and canopy cover (see also Lopes et al. 2005;
Mathura et al. 2005; Wilman et al. 2014; Collar et al. 2019).
Improvement in tree richness is related to the amount of feed-
ing resources available for birds (Kissling et al. 2007), which
may increase their abundance. Habitat requirements, such as
foraging stratum and feeding and nesting sites, may explain
the negative effects of tree richness and canopy cover on the
abundance of House Wren, Blue-black Grassquit, Eared
Dove, and Ruddy Ground-Dove. The last two are
synanthropic seed-eating species that forage on the ground
in open spaces (Fontoura and Orsi 2014), and have large pop-
ulations in urban landscapes in Brazil. These species have
behavioral plasticity and can tolerate human-made habitats,
such as using urban structures as support for their nests
Urban Ecosyst (2021) 24:375–390
(Guaraldo et al. 2015). The House Wren is a ground- arthro-
pod-eating bird that often inhabits several sites in urban set-
tlements (Redondo et al. 2013; Villaseñor and Escobar 2019).
This species may also have behavioral plasticity and may nest
in human-made cavities and structures (Marcondes-Machado
et al. 1994; Tyson et al. 2011; Zaldúa et al. 2013). Blue-black
Grassquit is a ground-seed eating species regularly found in
grassy open urban areas. Patches of native forests with less
canopy cover and tree richness supports the abundance of
these species because they fit some of their ecological require-
ments, such as increased open habitats. The results at the pop-
ulation level bring important insights for the conservation of
key ecological resources in native forest areas (tree richness
and canopy cover for low forest dependent species, Fig. 4).
We failed to detect any relationship between the sampled
environmental variables and bird body mass. The urbanization
process is a hierarchical filter that selects birds based on their
biological traits, like body mass (Croci et al. 2008a; Lizée
et al. 2011; Aronson et al. 2014), which can occur at both
landscape and local levels (Hostetler and Holling 2000). The
presence of larger wooded areas, and greater percentage of
tree cover, may be related to the presence of medium- to
large-bodied birds (Hostetler and Holling 2000). The areas
studied here would not provide suitable habitats for larger
species and were dominated by birds below 50 g. In fact, the
largest species detected was Picazuro Pigeon (Patagioenas
picazuro), which is adapted to city life (Leveau and Zuria
2017). The absence of larger-bodied species, due to the reduc-
tion of areas and resources needed for their maintenance, may
imply a reduction of important ecological functions, such as
the dispersion of larger seeds (Díaz et al. 2013; Emer et al.
2018) and the pollination of long-tubed flowers (Pauw and
Louw 2012). Thus, conserving larger areas would be an im-
portant strategy for enhancing ecological functions by main-
taining larger birds.
There was also no evidence of a relationship between for-
aging strata and vegetation variables, which may be linked to
the absence of understory in some of the areas (Online
Resource 1b). Urban greenspaces are known to have fewer
strata compared to rural and natural sites (Hedblom and
Söderström 2008), because understories and shrubs are usual-
ly cleared or depleted by managers for aesthetic, recreational
and public safety reasons (Heyman 2010). Clearing understo-
ry has a negative impact on species that depend on this stratum
(Pennington and Blair 2011; Heyman et al. 2017), since im-
portant vegetation components are being removed, such as
small trees and shrubs that can offer food (e.g., arthropods,
fruits and seeds), and partial defense from weather and pred-
ators (Paker et al. 2014).
Our results demonstrate that urban private native forest
fragments have vegetation characteristics that are as important
as riparian forests (Pennington and Blair 2011; Batisteli et al.
2018) and parks (Jokimäki 1999; Carbó-Ramírez and Zuria
Urban Ecosyst (2021) 24:375–390
2011; Zhou and Chu 2012; Jasmani et al. 2017), for driving
taxonomic diversity and functional traits of birds. Since pri-
vate greenspaces represent a significant proportion of the mo-
saic of urban ecosystems (Gaston et al. 2007; Davies et al.
2009), the results presented here support the protection of
natural vegetation structure not only in public areas, but in
private areas as well, due to their cascade effects on urban bird
composition, and the functions and services they provide.
These findings highlight the importance of urban private na-
tive forest fragments as reservoirs of urban biodiversity, and
bring important insights to ecological management with a fo-
cus on maintaining key ecological resources like the number
of standing dead trees and canopy cover, and prioritizing tree
diversity instead of solely abundance.
Acknowledgements We thank the National Council for Scientific and
Technological Development (CNPq) for the scholarship LACS (Process
nº132394 / 2016-2), and the administrations of the respective gated com-
munities who allowed us to access the study areas. We also thank Agnes
Leite Moreira, Willian Marcus Campos Silva and Márcia Aparecida
Campos Silva for help with data collection, Marcos Batalha, Mercival
Francisco and Eduardo Alexandrino for suggestions on an early version
of this manuscript, Marcos Melo, for help with statistical analyzes, and
the anonymous reviewers for their criticism and suggestions.
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