Urban Ecosystems (2021) 24:71–81

https://doi.org/10.1007/s11252-020-01021-2

Noise and tree species richness modulate the bird community

inhabiting small public urban green spaces of a Neotropical city
Beatriz Ferreira da Silva 1 & João Carlos Pena 2 & Arleu Barbosa Viana-Junior 3 & Matheus Vergne 4 &
Marco Aurélio Pizo 1

Published online: 17 June 2020

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

Abstract
Small public urban green spaces (SPUGS) are important for human life-quality and for maintenance of biodiversity within urban
landscapes. However, little is known about how local characteristics and spatial location are related to biodiversity inhabiting
SPUGS in tropical cities. In this study, we aimed at assess how noise, vegetation aspects (local characteristics), distance from a
major habitat patch and from water (spatial location) are related to the bird community (species composition, species richness,
total abundance and feeding guilds) inhabiting SPUGS in a medium-sized Neotropical city (Rio Claro, Brazil). We expected local
characteristics to be the most important variables influencing the bird community. Bird observations were conducted in 28
SPUGS (< 1 ha) and we used generalized linear models and a multi-model inference to assess the relationships between
SPUGS’ attributes and the bird community. Permutational multivariate analysis of variance was used to assess which SPUGS
characteristics modulate species composition. We made 1,808 records of 75 bird species distributed in 26 families. Noise was
negatively related to bird species richness, total abundance, and abundance of granivorous species. On the other hand, tree species
richness presented positive relationships with bird species richness and total abundance. Noise and tree species richness also were
responsible for modulating the composition of species inhabiting SPUGS. Therefore, we demonstrated that local characteristics
modulate birds inhabiting SPUGS; while noise is a strong limiting factor for birds inhabiting these small green spaces, increasing
tree species richness can enhance SPUGS’ ability in harboring a diverse bird community.

Graphical abstract
Representation of the outcomes of our study: in Rio Claro (São Paulo, Brazil), small public urban green spaces (SPUGS) nearby
quieter streets and with higher tree species richness harbor highly diverse bird communities. Noise was negatively related to bird
species richness, total abundance and abundance of granivorous bird species, while tree species richness presented positive
relationships with bird species richness and total abundance. This figure has been designed using resources from https://www.
Freepik.com

Keywords Bird feeding guilds . Medium-sized city . Species composition . Urban landscape . SPUGS

Electronic supplementary material The online version of this article

(https://doi.org/10.1007/s11252-020-01021-2) contains supplementary
material, which is available to authorized users.

* João Carlos Pena 2

Spatial Ecology and Conservation Lab (LEEC), Department of
joaocpena@gmail.com Biodiversity, Instituto de Biociências, Universidade Estadual Paulista
(UNESP), Rio Claro, São Paulo, Brazil
3
1
Laboratório de Ecologia de Aves (LECAVE), Department of Laboratório de Ecologia de Insetos, Programa de Pós-Graduação em
Biodiversity, Instituto de Biociências, Universidade Estadual Paulista Biodiversidade e Evolução, Coordenação de Zoologia, Museu
(UNESP), Rio Claro, SP, Brazil Paraense Emílio Goeldi, Belém, Pará, Brazil
4
Department of Biodiversity, Instituto de Biociências, Universidade
Estadual Paulista (UNESP), Rio Claro, São Paulo, Brazil
72
Introduction
In a world where urban landscapes are rapidly expanding and
harbor more than half of the human population (United
Nations 2018), it is fundamental to reconcile the development
and planning of cities with the preservation of biodiversity and
maintenance of ecological processes essential for the adequate
function of urban ecosystems, such as pest control and air
quality regulation (Kozlov et al. 2017; Schwarz et al. 2017).
To achieve such a goal, we need to plan and manage the green
infrastructure considering aspects that positively influence the
diversity and distribution of organisms in urban landscapes,
for instance the spatial configuration and plant species com-
position of green areas (Herzog 2013; Aronson et al. 2017).
Among the urban green infrastructure that can benefit both
people and wildlife are public urban green spaces (PUGS),
which are areas dominated by vegetation and permeable soil
that are accessible to all socioeconomic groups (Nucci and
Cavalheiro 1999). These areas comprise a range of habitat
types, from natural vegetation patches to managed parks and
green roofs, that can reduce pollution and noise, enhance hu-
man life-quality and provide shelter and resources for urban
biodiversity (Aronson et al. 2017, WHO 2017).
PUGS represent isolated vegetation patches within land-
scapes dominated by human-made structures, hence they are
fundamental for biodiversity conservation and maintenance of
ecological processes in cities (Aronson et al. 2014, 2017). Due
the high variability among PUGS’ types, biodiversity
inhabiting these spaces are influenced by several attributes
such as plant species composition, land use history, landscape
configuration and the surrounding urban matrix (Aronson
et al. 2017). Management strategies and intensity, such as
application of herbicides, removal of large and old trees, and
loss of vegetation strata hinder the ability of PUGS to harbor
native wildlife (Politi Bertoncini et al. 2012; Stagoll et al.
2012; Kane et al. 2015; Taylor et al. 2015; Zivanovic and
Luck 2016). To understand how environmental and landscape
attributes of PUGS are related to biodiversity, birds have been
used as models, since they comprise a highly diverse and
conspicuous group that respond to environmental modifica-
tions and constraints typical of urban landscapes (Marzluff
et al. 2001; Chace and Walsh 2006; Marzluff 2016). For ex-
ample, vegetation physiognomy and complexity of urban for-
est patches are highly different from peri-urban forests and
agricultural areas (e.g. shade-coffee plantations)
(MacGregor-Fors et al. 2018). These distinct conditions influ-
ence bird species composition especially during the breeding
season when habitat quality is especially important for the
occupation of vegetation patches (MacGregor-Fors et al.
2018).
Birds are able to exploit a variety of PUGS within the urban
matrix, including small-sized areas, such as squares (de
Toledo et al. 2012; Amaya-Espinel et al. 2019), pocket parks
Urban Ecosyst (2021) 24:71–81
(Ikin et al. 2013), and small greening projects in medium and
low-income neighborhoods underserved in vegetation cover
(Strohbach et al. 2013). These small (< 5 ha) PUGS (SPUGS)
usually are highly occupied by people that use these areas with
different purposes (e.g. passing through from one place to
another, exercising and socializing) (Peschardt et al. 2012).
In addition to befitting people, these small green spaces can
also positively influence bird communities. SPUGS harboring
trees with cavities that are located in greener and less dense
neighborhoods support higher bird species richness (Ikin et al.
2013; Strohbach et al. 2013; Amaya-Espinel et al. 2019).
Richness of insectivorous species within SPUGS increases
with the proximity to parks, while the diversity of granivorous
and introduced species increases in regions with higher pro-
portions of impervious surface (Strohbach et al. 2013). Native
vegetation diversity in SPUGS can enhance richness and
abundance of both sensitive and insectivorous bird species
(Amaya-Espinel et al. 2019). Despite the high similarity of
community composition between SPUGS and built-up envi-
ronments (Strohbach et al. 2013), all these relationships dem-
onstrate that local and landscape characteristics of SPUGS can
enhance their potential to harbor diverse bird communities.
Despite their importance in promoting human contact with
nature (Strohbach et al., 2013; WHO 2017) and their potential
to increase habitat and resource availability for birds in cities
(Aronson et al. 2017), the role of SPUGS and how their char-
acteristics affect urban bird communities require additional
information (Amaya-Espinel et al. 2019), particularly in trop-
ical countries and nearby biodiversity hotspots which com-
prise highly urbanized regions and/or regions with high rates
of urbanization (United Nations 2018). Since biodiversity in
cities contributes to maintaining human quality of life, a ho-
listic and integrated approach in planning and managing urban
green spaces with the aim of benefiting people and wildlife is
fundamental (Aronson et al. 2017).
The aim of this study was to assess how bird communities
in very small SPUGS (i.e. <1 ha) in a medium-sized
Neotropical city are related to local characteristics (noise and
vegetation) and the spatial location (distance from water and
from a major vegetation patch) of SPUGS. Our study city is in
the transition zone between two biodiversity hotspots –
Cerrado (Brazilian savanna) and Atlantic Forest. We will test
how bird species richness, total abundance, feeding guilds and
species composition are related to SPUGS’ characteristics.
Since ambient noise is a limiting factor for urban birds
(Perillo et al. 2017; Barbosa et al. 2020) and because the
SPUGS in our city are particularly small with many streets
nearby, we expected noise to be negatively related to bird
species richness, abundance and the diversity of feeding
guilds. Since vegetation characteristics of SPUGS (such as
the presence of native tree species) are positively related to
different aspects of bird communities, such as bird species
richness and abundance (Lerman and Warren 2011;
Urban Ecosyst (2021) 24:71–81
Strohbach et al. 2013; Amaya-Espinel et al. 2019), we expect-
ed local vegetation characteristics, such as density and rich-
ness of tree species, to be positively related to bird species
richness, abundance and the diversity of feeding guilds.
Considering that landscape configuration and the distance to
water also modulate bird communities inhabiting urban green
spaces (Aronson et al. 2017; Barbosa et al. 2020), we predict-
ed that the proximity to a major habitat patch and to water
would also be positively related to the characteristics of the
bird community inhabiting SPUGS. Furthermore, since insec-
tivorous and granivorous species present divergent relation-
ships with urbanization between Temperate and Neotropical
cities (Pena et al. 2017), we also investigated how these bird
groups are related to local characteristics and spatial location
of SPUGS. Finally, urban bird communities are highly influ-
enced by local environmental attributes (Pena et al. 2017).
Thus, we expected that local characteristics of SPUGS (noise
and vegetation) would also influence bird species
composition.
Materials and methods
Study area
The study was developed in Rio Claro (São Paulo, Brazil)
(22º26’ S, 47º31’ W) a medium-sized city with an estimated
population of 204,797 people (IBGE 2018). The climate is
characterized by a dry season between April and September,
and a wet season from October to March, with average annual
precipitation of 1479 mm (CEAPLA 2019). Rio Claro has a
diverse bird community, with 340 species, 12 of which are at
risk of extinction (Gussoni 2007).
Selection of SPUGS and bird survey
We selected 28 SPUGS (0.10–0.77 ha) distributed throughout
the urban landscape (Fig. 1). All SPUGS are at least 340 m
away from each other and are in different urban contexts, from
downtown areas surrounded by commercial buildings to
mostly residential areas nearby a state park, the Floresta
Estadual Edmundo Navarro de Andrade (FEENA) (Fig. 1).
FEENA is the largest forest patch in Rio Claro (2,222.80
ha), composed mostly by Eucalyptus plantations from differ-
ent species and ages and a few interspaced patches of hetero-
geneous native vegetation (mostly semideciduous seasonal
forest) (Fundação 2005). A total of 255 bird species have been
recorded at FEENA (Willis 2003).
Birds were surveyed by the same researcher (BFS) through
10-min point counts located at the center of each SPUGS. We
conducted a total of four counts at each location once every
two months from April to November 2018 so that two surveys
73
took place during the wet season and two during the dry sea-
son. To visit all 28 SPUGS, each survey period lasted approx-
imately two weeks (3–4 SPUGS were visited per day).
Sampling were performed between 7 a.m. and 10 a.m., only
in working days with favorable weather (sunny and non-
windy days) to avoid excessive variation in the circulation of
vehicles and people. To define the sampling order, the first
SPUGS was randomly selected and after it was sampled, we
walked to the next nearest SPUGS.
All birds that were visually detected within each
SPUGS were identified and the abundance of each species
was defined as the maximum number of records for each
species registered per site over the four visits (Lerman and
Warren 2011). We only recorded perched birds, excluding
from the analyses individuals that were only recorded fly-
ing above the SPUGS. Species were classified according
to the following feeding guilds: frugivorous/
nectarivorous, omnivorous, granivorous, carnivore/
detritivore and insectivorous (Wilman et al. 2014). We
pooled data from all four surveys to generate for each
SPUGS the species richness, total abundance of all birds
counted, the diversity of feeding guilds through
Shannon’s diversity index, and richness and abundance
of insectivorous and granivorous species, which were then
used as response variables (Online Resource 1).
Predictor variables
We selected seven predictor variables: two describing
SPUGS’ spatial location – Euclidian distance from the bor-
der of FEENA and from water bodies – and five local
characteristics – SPUGS’ size, tree species richness, pro-
portion of native tree species, tree density and noise
(Online Resource 1). We calculated the size of the
SPUGS and their spatial location using ArcGIS 10.4 soft-
ware. Noise was measured using the cellphone application
“Sound Meter” (ToolsDev 2016) as per Barbosa et al.
(2020). In each SPUGS, we measured the highest and low-
est noise levels (dB) during one minute before and one
minute after the bird survey (for a total of 8 min at each
site). During all surveys, we used the internal microphone
of the same smartphone (Galaxy S6 Edge - SM G925l) and
calibrated our ambient noise levels to reduce errors. We
then calculated the average sound level per SPUGS per
visit considering minimum and maximum readings and
we used the weighted average value of all visits as the
measure of noise exposure of each SPUGS. We surveyed
the tree species composition at each SPUGS in situ by
visual identification with the aid of published literature
(Harri 2003, 2008; Cardoso-Leite et al. 2014), and botanic
material was collected in case of uncertainties. We identi-
fied all trees and shrubs with height above 1 m and DBH >
10 cm.
74
Fig. 1 Small public urban green spaces (SPUGS) of Rio Claro (São
Paulo, Brazil) where we collected bird data, highlighting SPUGS in dif-
ferent contexts of the urban landscape. Low Dens. Build.: Low Density
Statistical analyses
We built generalized linear models (GLM’s) to assess the
relationships between SPUGS’ attributes and the bird commu-
nity and used multi-model inference to choose the best pre-
dictive and plausible model among all candidate models
(Burnham and Anderson 2002). The models were built based
on a single factor, (i.e. models containing a single predictor
variable) or the simultaneous action of the factors (i.e. models
containing a maximum of two of the predictor variables). Due
to the species-area relationship and the high correlation of
noise (r = -0.60, P < 0.05) and tree species richness (r = 0.71,
P < 0.05) with SPUGS size (Pena et al. 2020), we used
SPUGS size in all models as a blocking variable to control
for the variance attributable to SPUGS size. The remaining
predictor variables presented Pearson’s r < 0.50 assessed by
a pairwise comparison considering all variables (Online
Resource 2). Models with a discrete distribution (i.e. richness
and abundance) were built under Poisson errors, and continu-
ous response variables (i.e. Shannon diversity) followed
Gaussian errors. All models were then subjected to a model
selection.
Urban Ecosyst (2021) 24:71–81
Buildings; High Dens. Build.: High Density Buildings; Commercial
Build.: Commercial Buildings; Woody Veg.: Woody Vegetation;
Herbaceous Veg.: Herbaceous Vegetation
The relationships between predictor and response variables
were inferred based on the set of 22 models (i.e. one null, six
single factor, and 15 two-factor models) for each response
variable that differed by two or less units of AICc from the
best model (ΔAICc), thus capturing greater uncertainty in the
final set of candidate variables (Burnham and Anderson
2002). Model averaging was applied to make biological infer-
ence about the variables of which the averaged estimates did
not include zero within their standard-error range. This strat-
egy is important to identify uninformative parameters in sta-
tistical models applying model selection in ecology. An unin-
formative parameter is a predictor that has no relationship with
the response variable, making little to no improvement in the
log-likelihood of a model (i.e. model fit), but can be included
in a model ranked close to models with informative parame-
ters based on confidence intervals (Leroux 2019). We also
calculated the relative importance value (RIV) of each predic-
tor on the full model. The RIV is the sum of the Akaike
weights (probability of a model to be the most plausible
one) for the models in which each predictor appears.
Therefore, a predictor included in models with high Akaike
weights will receive a higher RIV value. These values can be
Urban Ecosyst (2021) 24:71–81
considered as the general support for each predictor variable in
all models. The 50% cut-off threshold is arbitrary and was
defined to differentiate important and unimportant predictors
(Burnham and Anderson 2002; Terrer et al. 2016; Deschutter
et al. 2017; Everaert et al. 2018). Finally, we built a presence-
absence matrix and used a permutational multivariate analysis
of variance (PERMANOVA) with Jaccard index to assess
which and how SPUGS characteristics modulate bird species
composition. We performed all analyses in the platform R (R
Core Team 2020) using the adonis function of the vegan
package for the PERMANOVA (Oksanen et al. 2019), the
aictab function of the AICcmodavg package for model selec-
tion (Mazerolle 2019), and the model.avg function of the
MuMIn package for model averaging (Barton 2019).
Results
We recorded 1,808 individual birds from 75 species and 26
families (Online Resource 3), which correspond to 21% of all
species recorded in Rio Claro. Tyrannidae was the most rep-
resentative family (16 species, 21.33%), followed by
Thraupidae (13 species, 17.33%). Together they account for
almost 40% of the recorded bird species. The most abundant
family was Columbidae (391 records), mainly due to the high
number of records of the most abundant species, the eared
dove Zenaida auriculata (217 individuals, or 12.00% of all
records) (Online Resource 3). The house sparrow Passer
domesticus was the second most abundant species, with 169
(9.34%) records (Online Resource 3). Overall, species rich-
ness varied from 9 to 36 species, and abundance from 21 to 94
records per SPUGS (all four counts pooled) (Online Resource
1). Considering feeding guilds, Shannon’s diversity index var-
ied from 1.04 to 1.53 (Online Resource 1). Insectivorous birds
accounted for 41.33% of the species, while 41.70% of all
records were granivorous, making them the most diverse
and abundant guilds, respectively. Among SPUGS, the rich-
ness of insectivorous birds varied from 3 to 16 species and
abundance from 5 to 42 records (Online Resource 1).
Richness of granivorous birds varied from 3 to 10 species
and abundance from 9 to 44 records (Online Resource 1).
When assessing how SPUGS characteristics are related to
the bird community, tree species richness presented the stron-
gest and positive relationship with bird species richness (this
predictor was included in all best ranked models), followed by
noise that was negatively related to this response variable
(Table 1; Figs. 2a and b). Noise presented a strong and nega-
tive relationship with total abundance, followed by a small
and positive relationship with tree species richness (Figs. 2c
and d). Considering the diversity of feeding guilds and the
richness of granivorous species, the null model was consid-
ered with substantial empirical evidence, thus any of the
assessed predictor variables were related to these aspects of
75
the bird community inhabiting SPUGS at Rio Claro (Table 1,
Online Resource 4). In relation to richness and abundance of
insectivorous species, although 13 models had substantial em-
pirical evidence (Table 1), all variables overlapped with zero
within their stand-error range and/or presented less than 50%
of RVI (Online Resource 4). On the other hand, noise present-
ed a strong and negative relationship with the abundance of
granivorous species (Fig. 2e and f) and was included in four
out of five models that presented substantial empirical evi-
dence (Table 1). Finally, we observed that noise (R² =
0.07348, P = 0.015) and tree species richness (R² = 0.11186,
P = 0.001), both describing local conditions, modulated the
composition of bird species inhabiting SPUGS (Table 2;
Fig. 3).
Discussion
We confirmed our expectations that local conditions – i.e. tree
species richness and especially noise – are responsible for
modulating the composition of bird species inhabiting
SPUGS. Noise is a strong limiting factor for birds inhabiting
cities (Pena et al. 2017; Perillo et al. 2017; Barbosa et al. 2020)
and in our study was negatively related to bird species rich-
ness, total abundance and abundance of granivorous species.
This is related to the small sizes of the green spaces we studied
(< 1 ha), leading to a high influence of the disturbances pro-
voked by the streets nearby. However, tree species richness is
positively related to community aspects, which may be indic-
ative of their ability to compensate for the negative effects of
noise (Pena et al. 2017). Therefore, SPUGS nearby quieter
streets and with higher tree species richness harbor abundant
and highly diverse bird communities.
In our study, the lowest noise level was 59dB, while the
average noise level was 66.75dB. The World Health
Organization recommends that noise levels produced by road
traffic should be below 53dB; higher levels are associated
with adverse human health effects, such as cardiac and mental
problems (WHO 2018). However, noise levels from 40dB
begin to affect bird communities, modifying species richness,
abundance, physiology, communication (frequency, duration
and complexity of vocalization), and reducing reproductive
success (Shannon et al. 2015). Noise can be considered a
selective pressure, negatively influencing bird species rich-
ness and diversity within urban parks (Perillo et al. 2017;
Barbosa et al. 2020). Due to the small sizes of SPUGS and
their proximity to streets, we expected a strong and negative
relationship between noise and the bird community inhabiting
these green spaces. Considering the small sizes, the high noise
76
Fig. 2 Model averaging of candidate models with ΔAICc < 2 for species
richness (A and B), total abundance (C and D) and abundance of
granivorous species (E and F) of the bird community inhabiting small
public urban green spaces (SPUGS) in Rio Claro (São Paulo, Brazil). The
average coefficients (± standard-errors) are presented on the left side and
levels, and the negative relationships we observed, we may
conclude that birds inhabiting SPUGS are probably as vulner-
able to human disturbances as birds inhabiting streets (Pena
et al. 2017).
Tree species richness in SPUGS presented positive rela-
tionships with bird species richness and total bird abundance.
Urban Ecosyst (2021) 24:71–81
the relative important values (RVI) of each predictor variable on the right
side. Since we used SPUGS size in all models as a blocking variable, it
appears in all models (RVI = 1.0), but without a coefficient of
determination
This was already observed for birds inhabiting streets at an-
other Neotropical city (Pena et al. 2017), indicating that char-
acteristics of the urban afforestation process can reduce the
negative effects of noise exposure on birds. Higher tree spe-
cies richness probably increase the ability of SPUGS to harbor
a higher diversity of resources (Faeth et al. 2005; Burghardt
Urban Ecosyst (2021) 24:71–81
Fig. 3 Species occurrences in relation to different values of tree species richness (on the left) and noise levels (on the right) in small public urban green
spaces (SPUGS) in Rio Claro (São Paulo, Brazil)
et al. 2009; Narango et al. 2017), leading to a positive rela-
tionship with bird species richness. Other local vegetation
characteristics of SPUGS, such as tree and shrub cover, also
have positive influences on bird communities (Ikin et al. 2013;
Strohbach et al. 2013). Furthermore, native trees were already
demonstrated to be positively related to bird species richness
and abundance of insectivorous birds inhabiting SPUGS
(Amaya-Espinel et al. 2019). Therefore, the planning and
management of the urban afforestation process has the poten-
tial to mitigate some of the negative impacts of urbanization
on birds within the urban matrix.
None of the assessed predictors were considered plausible
for explaining the variation in richness of granivorous and
insectivorous bird species. Maybe other factors, such as plant
species composition and characteristics of the surrounding
urban matrix (e.g. proportion of green cover), may influence
the diversity of these feeding guilds (Ikin et al. 2013;
77
Strohbach et al. 2013; Amaya-Espinel et al. 2019).
Furthermore, most species classified in our study as insectiv-
orous and granivorous are commonly found in Brazilian cities,
especially in the southeast: the eared dove (Zenaida
auriculate), the ruddy ground-dove (Columbina talpacoti),
and the picazuro pigeon (Patagioenas picazuro) as examples
of granivorous species; the variegated flycatcher
(Empidonomus varius), the cattle tyrant (Machetornis rixosa),
the southern house wren (Troglodytes musculus), and the
chalk-browed mockingbird (Mimus saturninus) among insec-
tivores (Pena et al. 2017; Perillo et al. 2017; Barbosa et al.
2020; Guimarães et al. 2020). These species may be classified
as urban exploiters (Blair 1996), efficiently moving through
the urban landscape in search of adequate areas for their daily
activities. On the other hand, abundance of granivorous spe-
cies presented a strong and negative relationship with noise.
This result is probably related to foraging behaviour: most
78 Urban Ecosyst (2021) 24:71–81

Table 1 Models with substantial empirical evidence (Δ ≤ 2) when assessing the relationships between SPUGS (small public urban green spaces)
characteristics and species richness, abundance and feeding guilds within the urban landscape of Rio Claro (São Paulo, Brazil)

Response variable Models k LogLik AICc Δ Weight

Species richness
Poisson Noise + Tree richness 4 -85.88 181.50 0.00 0.51
Water distance + Tree richess 4 -86.55 182.84 1.34 0.26
FEENA distance + Tree richness* 4 -88.30 186.35 4.84 0.05
Individuals abundace
Poisson Noise + Tree richness 4 -122.75 255.23 0.00 0.47
Noise* 3 -125.26 257.52 2.29 0.15
Shannon diversity
Gaussian Null 2 24.18 -43.89 0.00 0.43
Water distance* 4 25.42 -41.09 2.79 0.10
Insectivorous richness
Poisson Noise + Tree richness 4 -66.37 142.47 0.00 0.25
Noise 3 -68.48 143.96 1.48 0.12
Tree richness 3 -68.73 144.46 1.99 0.09
FEENA distance + Tree richness* 4 -67.60 144.93 2.46 0.07
Insectivorous abudance
Poisson Native richness (%) 3 -89.63 186.26 0.00 0.11
Noise 3 -89.74 186.49 0.23 0.10
Tree density 3 -89.79 186.58 0.32 0.09
Water distance 3 -90.02 187.04 0.78 0.07
Tree density + Tree richness 4 -88.72 187.17 0.91 0.07
FEENA distance 3 -90.26 187.52 1.25 0.06
Tree richness 3 -90.28 187.55 1.29 0.06
Tree density + Noise 4 -89.04 187.82 1.56 0.05
Noise + Native richness (%) 4 -89.09 187.92 1.66 0.05
Tree density + Native richness (%) 4 -89.10 187.94 1.67 0.05
Tree density + Water distance* 4 -89.30 188.35 2.09 0.04
Granivorous richness
Poisson Null 1 -56.85 115.86 0.00 0.39
Noise* 3 -56.07 119.14 3.27 0.08
Granivorous abudance
Poisson Noise + Native richness (%) 4 -100.21 210.15 0.00 0.22
Noise 3 -102.00 210.99 0.84 0.14
FEENA distance + Noise 4 -100.93 211.61 1.45 0.10
Water distance + Noise 4 -101.08 211.91 1.75 0.09
Native richness (%) 3 -102.51 212.02 1.87 0.09
FEENA distance* 3 -103.00 213.00 2.85 0.05

k = number of parameters in the model, Loglik = log-likelihood, AICc = second-order Akaike information criterion, Δ = AICc difference between the
model under concern and the best model, Weight = Akaike weight, i.e. the likelihood of the model being the best in the set of candidate models. SPUGS
size was included in all candidate models
*Models included to demonstrate the ΔAICc values between models with and without substantial empirical evidence

granivorous birds recorded in our study are gregarious and
ground foraging species. Although abundant throughout the
assessed SPUGS, granivorous birds are probably more vul-
nerable to disturbances related not only to traffic volume, but
to ground dwelling predators (e.g. cats) and people using these
green areas for different purposes (Croci et al. 2008; Jokimäki
et al. 2016). Thus, SPUGS located in regions with high traffic
volume harbor less individuals of granivorous birds in con-
trast to sites nearby quieter streets. On the other hand, most
insectivorous birds are flycatchers and/or forage on the tree
canopy and are probably less affected by anthropogenic dis-
turbances of SPUGS.
Urban Ecosyst (2021) 24:71–81
Table 2 Results of the permutational multivariate analysis of variance
(PERMANOVA) to assess which SPUGS (small public urban green
spaces) characteristics modulate the bird community composition
inhabiting these green spaces in Rio Claro (São Paulo, Brazil)
Explanatory variable Sums of Squares F.Model R²
FEENA distance 0.238 1.455 0.053
Water distance 0.245 1.496 0.054
Tree richness 0.503 3.275 0.112
Native tree (%) 0.151 0.902 0.034
Noise 0.330 2.062 0.073
Tree density 0.166 0.999 0.037
Variables in bold highlight significant results
The diversity of feeding guilds did not present statistically
supported relationships with the assessed SPUGS characteris-
tics. Maybe due to their small sizes, we did not observe a large
variety of food resources among SPUGS. On the other hand,
other local conditions related, for example, to vegetation struc-
ture and complexity, would highlight differences on bird feed-
ing guilds between these sites (Faeth et al. 2005; Burghardt
et al. 2009; Lerman and Warren 2011; Ikin et al. 2013;
Strohbach et al. 2013; Narango et al. 2017). Resources avail-
able in the vicinity of SPUGS, such as a large forest patch or
water resources, could lead to positive influences on bird feed-
ing guilds. For example, lower temperatures in urban areas
nearby waterbodies attenuate the influences of the heat island
effect within cities, positively influencing resources such as
abundance of arthropods and plant growth (Leveau 2018;
Barbosa et al. 2020), what can probably lead to a higher di-
versity of feeding guilds. However, the SPUGS in Rio Claro
represent islands of vegetation immersed into a matrix of im-
permeable surfaces with almost a lack of roadside vegetation
and street trees (Pena et al. 2020). This characteristic of Rio
Claro may hinder the ability of some bird species with restric-
tive habitat requirements to exploit other green spaces, being
restricted to peri-urban areas and regions, such as FEENA.
Thus, the reduced permeability of Rio Claro’s landscape
may explain the absence of statistically supported relation-
ships between the characteristics describing the spatial loca-
tion of SPUGS and the bird community.
Since noise and tree species richness presented negative and
positive relationships with aspects of the bird community
inhabiting SPUGS, respectively, they were also considered the
most important predictors modulating species composition.
Some species only occurred in SPUGS with high tree species
richness, while others did not occur in the noisiest SPUGS.
However, most species were observed in SPUGS with almost
all the variation of these conditions. This explained the small
values of the coefficients of determination (R² = 0.07348 for
noise; R² = 0.11186 for tree species richness) and demonstrated
that the studied community is mostly comprised by urban
79
exploiters. Nevertheless, this result did not hinder the importance
of SPUGS in conserving a high diversity of bird species. These
green areas harbor migratory species – e.g. the streaked flycatch-
er (Myiodynastes maculatus) and the fork-tailed flycatcher
Pr(> F) (Tyrannus savana) – and we recorded some frugivorous/
0.091
nectarivorous and insectivorous species only in SPUGS with
0.092
high tree species richness, for instance the toco toucan
(Ramphastos toco), the amethyst woodstar (Calliphlox
0.001
amethystine) and the little woodpecker (Veniliornis passerinus).
0.542
0.015
0.450
Conclusions
In an urbanized world with an increasing need of accommodating
a growing human population, we need to understand how envi-
ronmental attributes and landscape configuration of cities affect
biodiversity inhabiting the urban matrix. Even being small and
under high influence of traffic noise, SPUGS are important for
human wellbeing and quality of life and we demonstrate that their
vegetation characteristics can also positively influence urban bird
communities. Tree species richness and noise exposure modulate
bird species composition and may describe the quality of SPUGS
as habitat for birds. Granivorous birds, characterized in our land-
scape most by gregarious and ground-foraging species, may be
more vulnerable to the traffic volume in the streets nearby, leading
to a negative relationship between noise and abundance of this
feeding guild. The low permeability of Rio Claro’s landscape
may explain the absence of statistically supported relationships
between spatial location (distance to water and FEENA) and the
bird community. Therefore, planning and managing practices of
green areas such as SPUGS need to have a holistic approach,
considering not only local conditions (e.g. vegetation characteris-
tics, management practices), but also different scales (local, neigh-
borhood, city) and the responses and needs of both human and
non-human organisms inhabiting urban landscapes.
Acknowledgements BF da Silva and JC Pena were supported by São
Paulo Research Foundation (FAPESP) (Grants: 2017/26145-6,
2018/00107-3, 2018/22215-2). AB Viana-Junior received a postdoctoral
scholarship from the Biodiversity Research Consortium Brazil-Norway
(BRC), Hydro-Alunorte (#12/16 Ecological Interaction project). MA
Pizo receives a research grant from the Brazilian Research Council
(CNPq).
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