Vol.:(0123456789)
Environment, Development and Sustainability
https://doi.org/10.1007/s10668-020-00993-7
1 3
Preservation ofhistorical heritage increases bird biodiversity
inurban centers
TulaciBhakti
1
· FernandaRossi
1
· PedrodeOliveiraMaa
1
·
EduardoFrancodeAlmeida
1
· MariaAugustaGonçalvesFujaco
2
·
CristianoSchetinideAzevedo
1
Received: 16 April 2020 / Accepted: 16 September 2020
© Springer Nature B.V. 2020
Abstract
Urban expansion negatively influences biodiversity by eliminating habitats and homoge-
nizing the biotic component, to which many species are unable to respond. However, his-
torical cities, with their protected heritage sites, maintain many fragments of vegetation
(gardens, squares, etc.). Such fragments permit the existence of biodiversity, especially of
birds, because they provide areas for shelter and food and function as stepping stones that
increases the permeability of the urban matrix. We hypothesized that the presence of green
areas, such as gardens and parks, would favor greater richness and abundance of bird spe-
cies, especially omnivores and granivores, during the dry season and in the Historic Center
of the city of Ouro Preto. Birds were sampled by point counts at 35 points distributed
throughout the urban matrix of Ouro Preto, where richness and abundance were recorded
and correlated with land use. Both the presence of green areas and the maintenance of the
Historic Center influenced the bird community present in the urban center, with higher
richness in areas with more shrubs and trees and closer to larger forested fragments. Bird
abundance was greater in the Historic Center and during the rainy season. These findings
demonstrate that maintaining heritage sites in urban centers can mitigate the expected neg-
ative impacts of urbanization by allowing small patches of vegetation to serve as favorable
habitats for bird species.
Keywords Avifauna· Abundance· Conservation· Historical center· Richness·
Urbanization
1 Introduction
Urbanization transforms both the physical and biotic structures of a given habitat and can
interfere with various ecological processes that involve local fauna and flora (Mendonça
and Anjos 2005). Such modifications result in a landscape composed of a mosaic of envi-
ronments, with floristic composition and structure usually different from those originally
* Cristiano Schetini de Azevedo
cristianorox[email protected]; cristiano.azevedo@ufop.edu.br
Extended author information available on the last page of the article
T.Bhakti et al.
1 3
present (Grimm etal. 2008; Patra etal. 2018). These mosaics are diffuse with patches of
native vegetation interspersed by areas with different levels of human occupation (Marzluff
etal. 2001; Yi etal. 2016).
Biodiversity can be directly or indirectly affected by urbanization (McDonald et al.
2019; Turrini etal. 2016). Direct effects are observed when a natural area is replaced by
an urban area with the construction of buildings, houses, or other human modifications
(Pejchar etal. 2015). All the changes that occur to biotic and abiotic conditions in a newly
urbanized environment, such as modifications to temperature, light, and wind (Beninde
etal. 2015; McDonald etal. 2013), as well as reductions in connectivity among vegetation
fragments and increased edge effects, are also considered direct effects of urbanization on
biodiversity (Concepción etal. 2015; Schneider etal. 2015; Veselkin etal. 2018). Pollu-
tion produced by urban areas and the resources needed for the correct functioning of the
city, like energy and food, are considered indirect impacts of urbanization on biodiversity
(McDonald etal. 2019; Turrini etal. 2016).
The effects of urbanization can be evaluated by the impacts on local biodiversity, such
as birds (Ikin etal. 2012; Ortega-Álvarez and MacGregor-Fors 2009). Birds are commonly
dependent on local environmental characteristics and are often used to measure the degree
of urbanization (Fontana etal. 2011; Møller etal. 2015; Ortega-Álvarez and MacGregor-
Fors 2009; Rodrigues etal. 2018). Birds are excellent models for studying the impacts of
urbanization and fragmentation because they are easily observed in cities, their taxonomy
is well defined and they present high species and functional richness and thus are consid-
ered good bioindicators for habitat quality (Anjos etal. 2015; Li Yong etal. 2011; Powell
etal. 2015). In this way, it is possible to use characteristics of species, such as food prefer-
ences, and characteristics of the urban landscape, such as the degree of urbanization and
the presence of vegetated areas, to assess how an urban center acts as a filter for bird spe-
cies (Ikin etal. 2012; Silva etal. 2016).
Different trophic guilds of birds can respond differently to urbanization (Cristaldi etal.
2017; Evans etal. 2011; Sol etal. 2014). Granivorous and omnivorous species are more
common in urban areas because they feed on food items that are abundant there (e.g., grass
seeds are common in cities) or have a more generalist diet and consume a wide range of the
available food items, including human-industrialized food wastes (Croci etal. 2008). More
specialized bird guilds, like frugivores and insectivores, are rarer in urban environments
because they normally occur in larger green areas that provide more food and specific habi-
tats (Cristaldi etal. 2017; Silva etal. 2016).
Urbanization can increase the abundance of several species, but it usually reduces total
richness (Chace and Walsh 2006). Due to the changes in conditions that urbanization of
environments brings, many species become extinct, which leads to biotic homogenization
(Blair 2008). On the other hand, there are indications that the maintenance of green areas
in cities, such as parks, squares and trees on public roads, favors the occurrence of bird
species in urban areas (Barth etal. 2015; Castro Pena etal. 2017). Even though they are
small, birds use these green areas as habitat or as stepping stones (small green areas used
as a resting place when traveling to larger green areas; Boscolo etal. 2008; Metzger 2001).
These small fragments can allow greater permeability of species into urban landscapes
(Baum etal. 2004; Bhakti etal. 2018; Fischer and Lindenmayer 2002), by making con-
nections with other fragments of vegetation located in peri-urban areas (Ikin etal. 2013;
Manhães and Loures-Ribeiro 2005).
Landscapes of cites are continuously changing, with new urban areas being added as cit-
ies grow (Farrell 2017). Green areas within cities also change, often being excluded from
the matrix after renovations (Mensah 2014). However, there are cities that are considered
Preservation ofhistorical heritage increases bird biodiversity
1 3
historical heritage, whose green areas tend to remain in the urban matrix for longer periods
of time since no radical renovations are permitted (Rostami etal. 2015). Such a scenario
would allow the persistence of old green areas within urban areas, which could play a role
in the preservation of biodiversity by experiencing less anthropic disturbance (Ferreira
etal. 2013).
The maintenance of such older green areas has the potential to maintain greater biodi-
versity since their age has allowed sufficient time for plant–animal interactions to become
established, with bird communities being composed of less sensitive and more urban-
adapted species in these older green areas (Castro Pena etal. 2017; Eriksson 2016; Threl-
fall etal. 2017). Connectivity among fragments, as well their sizes and shapes, can permit
mobility and interchange of birds through the city matrix (Caneva etal. 2020; Parris etal.
2018). If fragments are closer to environmentally protected areas, they can increase the
permeability of a city for birds (Bhakti etal. 2018; Parris etal. 2018). Thus, greater rich-
ness and abundance of bird species are expected in green areas of historical heritage cities.
Bird communities can change seasonally due to the influences of weather and produc-
tivity (Seoane etal. 2013; Seress and Liker 2015). During the dry season, for example,
when food availability decreases, many migrant species leave an area in search of more
suitable places (Lepczyk etal. 2017; Leveau 2018). However, the environment of a city is
more homogeneous than natural environments, including less fluctuations in food availabil-
ity (Seress and Liker 2015; Tryjanowski etal. 2015). Thus, changes in bird communities
of cities are especially expected during the dry season because more bird species and indi-
viduals will seek resources within the urban matrix, thereby increasing bird richness and
abundance (Caula etal. 2008, 2014).
Thus, the present study aimed to evaluate the composition, richness, abundance, trophic
guilds, and frequency of occurrence of bird species in the urban area of Ouro Preto, a his-
toric city located in the Atlantic Forest biome of Brazil. We also evaluated the effects of
seasonality on the urban bird community and how the degree of urbanization influences
the richness and abundance of birds. Lastly, we compared bird richness and abundance
between historic and newly urbanized areas in the city using the Special Protection Zone
defined by the Master Plan of the city as a parameter.
We hypothesized that (1) the presence of green areas, such as gardens and parks, would
favor greater richness and abundance of bird species, especially of omnivores and grani-
vores; (2) there would be greater richness and abundance of birds in the city during the dry
season because more bird species and individuals will seek resources there; (3) areas with
a greater degree of urbanization will have lower bird richness and abundance; and (4) there
will be greater bird richness and abundance in historic protected zones. The results of this
study could assist managers in making decisions for the future growth of the city, through
the identification of priority areas for bird protection.
2 Research methodology
2.1 Study area
Recognized as Intangible Cultural Heritage of Humanity since 1980 by UNESCO, the
municipality of Ouro Preto (20° 23 28 S, 43° 30 20 W; Minas Gerais State, southeast-
ern Brazil) has a large urban heritage site. This situation allowed the maintenance of the
original urban structure, including a park, Horto do Contos, opened in 1799 in the central
T.Bhakti et al.
1 3
region (Pereira 2015). Horto do Contos is located within a protection zone that preserves
the region where the city originated, called the Special Protection Zone, that was deter-
mined by the city’s Master Plan (Ouro Preto 2006). Based on this, levels of protection and
maintenance of the regions structure were defined, which prevent major urban and con-
struction changes in the region in the heritage site.
2.2 Bird sampling
Birds were sampled by listening point counts at 35 counting points located on city streets
and distributed at least 300m from each other along the urban perimeter of Ouro Preto (as
determined by local legislation; Ouro Preto 2006) (Fig.1). Bird species and their abun-
dances were recorded at each point during 20-min sampling periods (Vergara etal. 2010;
Vielliard et al. 2010; Volpato etal. 2009). Sampling was carried out monthly between
August 2013 and December 2014 (except April and May 2014), between 6:00 and 9:00am,
for a total of 98days. The order that counting points were sampled was changed on each
sampling day so that all points were sampled equally at each hour of sampling (6:00 to
9:00am).
Bird species were classified according to their food preference (Lopes et al. 2005a,
2005b; Sabino etal. 2017; Schubart etal. 1965) (Table1), as well as their degree of end-
emism in relation to the Atlantic Forest biome (Vale etal. 2018). Scientific nomenclature
followed the rules of the Brazilian Committee for Ornithological Records (Piacentini etal.
2015). Bird richness was estimated by first-order Jackknife using EstimateS 8.2 software
Fig. 1 Location of the city of Ouro Preto (Minas Gerais State, southeastern Brazil), showing land use (a)
and the distribution of counting points (b) in the urban area of the city
Preservation ofhistorical heritage increases bird biodiversity
1 3
(Colwell 2009). This estimate is based on the number of sampling units (each point count)
used and the presence or absence of species at each point (Develey 2003).
2.3 Data analysis
A map of coverage and land use provided by the Municipal Secretariat of Heritage of Ouro
Preto (Quickbird 2003 and 2006) was used for landscape analysis. The map divided the
urban perimeter into five classes: tree vegetation, shrub vegetation, herbaceous vegetation,
Eucalyptus vegetation, built area and exposed soil (Fig.1). To assess the presence of each
class at the counting points, 600m buffers were established and the proportion of each
class in the buffer was subsequently calculated. In addition, the size of the nearest forest
fragment and the distance of the nearest forest fragment were calculated for each count-
ing point. The proportion and the size and distance of the fragment closest to the counting
points (predictive variables) were related to bird species richness and abundance (response
variables) using Generalized Linear Models (GLMs).
Kernel density estimators (KDEs, Węglarczyk 2018) seek to estimate densities based
on local information, instead of estimating global parameters for data models. They use a
group of density probability functions called kernels, which produce a usage distribution
(He etal. 2020). Such estimators perform a count of all points within a region of influ-
ence, weighting them by the distance between points. A kernel is considered accurate at
assessing the distribution of the locations of individuals (Jacob and Rudran 2003; Laver
and Kelly 2008). KDEs were estimated to determine the areas within the city of Ouro Preto
that possesses the greater richness and abundance of birds. Values of kernel density were
classified according to density level, for species richness and abundance, through the Natu-
ral Breaks method of ArcGIS software, to guarantee maximum difference between gener-
ated classes (Baz etal. 2009).
The influence of season (dry and rainy seasons) and the Special Protection Zone (his-
torical sites and new areas) (predictive variables) on bird richness (response variable) was
evaluated by constructing Generalized Linear Mixed Models (GLMMs). Complementa-
rily, Permutational Analysis of Variance (PERMANOVA) was used to determine whether
species composition varied between seasons. The dry season was considered between the
months of April and September and the rainy season between the months of October and
Table 1 Feeding guilds, and their characteristics, used to classify bird species found within the urban
perimeter of the city of Ouro Preto
Feeding guild Characteristics
Insectivores (INS) Species whose diet consists of three-fourths or more of insects and other arthro-
pods
Omnivores (ONI) Species whose diet is composed of plant and animal material in similar propor-
tions
Frugivores (FRU) Species whose diet consists of three-fourths or more of fruits
Granivores (GRA) Species whose diet consists of three-fourths or more grains
Nectarivores (NEC) Species whose diet is predominantly composed of nectar, but also includes insects
and other arthropods
Carnivores (CAR) Species whose diet consists of three-fourths or more of live vertebrates
Necrophages (NECRO) Species whose diet consists of three-fourths or more of dead animals
Piscivores (PIS) Species whose diet is predominantly composed of fish
T.Bhakti et al.
1 3
March. Permutational Analysis of Multivariate Dispersion (PERMDISP) was performed to
measure data dispersion. The graphic representation of variation in the composition of bird
species between seasons was done using Non-metric Multidimensional Scaling (NMDS).
All analyses were performed using R software version 3.1.0 (R Development Core Team
2015).
3 Results
One hundred and fifty-one bird species representing 39 families and 18 orders were
recorded during a total of 294 sampling hours (TableS1 Supplementary material). The
most represented order was Passeriformes with 97 species, corresponding to 64.2% of
all registered species. The most represented passeriform family was Tyrannidae with 29
species (19.2%), followed by Thraupidae with 27 species (17.9%). Apodiformes was the
next most represented order, with the family Trochilidae having ten species (6.6%). The
observed bird species richness was 86.29% of the estimated richness for the urban perim-
eter of Ouro Preto (species accumulation curve in Fig. S1 Supplementary material).
There was a predominance of insectivorous bird species (63 species, 42%), followed
by omnivores (37 species, 24%), granivores (14 species, 9%), frugivores (13 species, 9%),
nectarivores (11 species, 7%), carnivores (nine species, 6%), piscivores (three species, 2%),
and necrophages (one species, 1%).
The highest values found for kernel density for both richness and the abundance of
bird species were in the region around Horto dos Contos (Fig.2), which is in the Historic
Center of the city of Ouro Preto.
Fig. 2 Kernels built to show the areas with the greatest richness (a) and abundance (b) of bird species
within the urban perimeter of the city of Ouro Preto (in red), Minas Gerais, Brazil. The black line indicates
the Special Protection Zone (a, b, c), while the orange line indicates the area of Horto dos Contos (c)
Preservation ofhistorical heritage increases bird biodiversity
1 3
Twenty of the recorded species are considered endemic to the Atlantic Forest biome
(Table S1 Supplementary material), including Aramides saracura, Florisuga fusca,
Leucochloris albicollis, Pyriglena leucoptera, Lepidocolaptes squamatus, Mionectes
rufiventris, Knipolegus nigerrimus, Turdus subalaris, and Tangara desmaresti. Only the
species Sporophila frontalis was present on the list of endangered animals of Brazil,
with the status of Vulnerable (MMA 2014). This species was registered only in Horto
do Contos.
The following positive results were found for the analysis of buffers with the soil
cover and for the size and distance of the nearest forest fragments in relation to the
counting points: (1) bird species richness: herbaceous vegetation (F = 11.67 and
p < 0.001) (Fig.3a) and tree vegetation (F = 26.28 and p < 0.001) (Fig.3b); (2) bird spe-
cies abundance: herbaceous vegetation (F = 12.04 and p < 0.001) (Fig.3c) and tree veg-
etation (F = 24.37 and p < 0.001) (Fig.3d). There was a significant relationship between
bird abundance and proximity to the nearest forest fragment (F = 7.97 and p = 0.005).
All other relationships tested were not significant.
Bird richness was significantly related to seasonality (DF = 1; X
2
= 5.29, p = 0.021)
(Fig.4a), with greater richness during the rainy season. No significant seasonal changes
in bird abundance were observed (Fig.4a). A comparison of the species composition
of bird communities between seasons revealed two distinct groups, one for each season
(PERMANOVA: Season: DF = 1; r2 = 0.26, p = 0.001; PESMIDISP: DF = 1; F = 17.46,
p < 0.001) (Fig.4b).
Bird richness was lower in the Special Protection Zone (Historic Center; T = 38.63
and p < 0.001), while bird abundance was lower at counting points outside the Special
Protection Zone (newly urbanized areas: T = 13.24 and p < 0.001).
Fig. 3 Positive relationships between bird richness and the amount of herbaceous (a) and tree (b) vegeta-
tion, and between bird abundance and the amount of herbaceous (c) and tree vegetation (d) in the city of
Ouro Preto
T.Bhakti et al.
1 3
4 Discussion
All of the evaluated parameters influenced, to some degree, bird species richness and abun-
dance. The presence of green areas influenced the urban bird community, with greater rich-
ness and abundance of bird species in areas with more herbaceous plants and trees. Addi-
tionally, bird species abundance increased with increasing proximity of forest fragments.
The urban bird community of Ouro Preto changed seasonally with greater richness during
the rainy season. Increasing degree of urbanization negatively influenced bird species rich-
ness and abundance, with more bird species and individuals in less urbanized areas, such
as Horto dos Contos. Finally, the Historic Center had lower bird richness but higher bird
abundance than did newly urbanized areas. This result demonstrates that maintaining green
spaces in urban centers can mitigate the expected negative impacts of urbanization since
small patches of vegetation can serve as favorable habitats for bird species. In the case of
Ouro Preto, the area located within the Historic Center has experienced little change to its
structure since 1950 (Oliveira 2004). Thus, the shape and number of buildings (i.e., how
much they occupy within the lots) have remained practically fixed, including backyards,
vegetable gardens, and other green areas, which favors the occurrence of bird species on a
local scale (Bhakti etal. 2018).
This argument is corroborated by the presence of a greater density of bird richness and
abundance near Horto dos Contos, which is in the Historic Center of the city. However,
when only bird richness and abundance are evaluated, the central region had more birds
(greater abundance), but fewer species (less richness). Although this result seems contra-
dictory, when evaluating the results of the kernel analysis, it is possible to observe that the
greatest richness and abundance were concentrated almost exactly in the area of Horto dos
Contos, reaching areas out of the Special Protection Zone (Fig.2). Horto dos Contos rep-
resents an old protected forested area with minimal management of the vegetation, which
is important for maintaining local diversity (Kümmerling and Müller 2012). Thus, Horto
dos Contos has greater structural complexity and larger microenvironments than do back-
yards and squares in the same area, facilitating the occurrence of a greater richness of bird
species. Furthermore, this area practically functions as an ecological corridor linking the
Historic Center to green protected areas throughout the city.
The greater abundance of birds in the Historic Center could also be related to the pres-
ence of a greater number of nesting and foraging areas. Roof ceilings, gaps between old
beams, chimneys, architectural pieces on old church facades and old, vegetated windowsills
Fig. 4 a Differences in bird richness and abundance between the dry season and the rainy season in the city
of Ouro Preto (different letters indicate significant differences between seasons). b Bird species composition
in the dry season (circles) and in the rainy season (triangles) in the city of Ouro Preto
Preservation ofhistorical heritage increases bird biodiversity
1 3
can be nesting sites for several of the species observed in the Historic Center of Ouro Preto.
Gardens and backyards, full of ornamental plants, can be feeding places for frugivorous,
granivorous, insectivorous, and nectarivorous birds. The presence of nesting and forag-
ing areas was related to a greater richness and abundance of birds in farmlands of Poland
(Rosin etal. 2016). On the other hand, the modernization of buildings in cities of Poland
decreased by 50% the abundance of building-nest birds (Rosin etal. 2020), showing that
new areas in cities can negatively impact the avifauna. A decrease in bird abundance out-
side the Historic Center was also observed in the present study.
Measures of species richness in urban environments are relevant for understanding the
different stages of landscapes that are responsible for the impoverishment of biological
diversity (Clergeau etal. 2002; Melles etal. 2003). Therefore, assessing the permeability
of an urban area is important, which we emphasize here with the large number of bird
species found (151). We associate this large number of bird species with the presence of
areas with herbaceous and tree vegetation, which was more important than the presence of
other land coverings, including urbanized areas, to the maintenance of birds. The number
of species associated with herbaceous and tree vegetation also reinforces the positive role
of heterogeneous environments for conserving biodiversity and reducing homogenization
of the urban bird community (Callaghan etal. 2019; Castro Pena etal. 2017; Chang and
Lee 2016).
Another important parameter that may be contributing to the high richness and abun-
dance of birds within the urban perimeter of Ouro Preto is the presence of large Conserva-
tion Units adjacent to the city (Silva etal. 2015). These units may act as source fragments
for birds that occur within the urban area, resulting in an increase in the richness and abun-
dance of birds (Casas etal. 2016), especially if there are green areas that allow this con-
nection (Snep etal. 2006). This point is highlighted by the increase in species richness and
abundance in the most distant points from the central region, which are close to peri-urban
areas, in addition to the relationship between the occurrence of bird species and the size
of the nearest forested area. Thus, peri-urban regions can play a role as strategic areas for
protection, mainly because they are areas that suffer great impacts from the growth of cities
(Aguilar 2008).
The Atlantic Forest has been reduced to just 10% of its original coverage, with most of
the remaining fragments being small and altered (Harris and Pimm 2004). Given to this
drastic reduction in forest cover and the high number of endemic bird species found in the
study area, we showed that the sampled landscape has important characteristics for the per-
sistence of species in the biome (Aronson etal. 2014; Plass and Jr 2013). This result sug-
gests the importance of assessing local biodiversity for urban planning and that city growth
must consider the presence of large areas of tree and herbaceous vegetation, as these are
capable of acting as areas of refuge for local avifauna.
Seasonality influenced the dynamics of the urban bird community in Ouro Preto, with
a positive correlation between species richness and the rainy season. This result was not
expected since increases in bird richness and abundance are generally observed in cities
during the dry season (Asefa etal. 2017; Girma etal. 2017). In the dry season, a period
of resource scarcity, changes in weather have greater influences on species in natural areas
because competition for resources increases, which may not occur in urbanized environ-
ments (Coogan etal. 2018; Ferger etal. 2014; Mulwa etal. 2013). Some species may find
urbanized areas attractive during times of adversity since the resources made available by
human activity are abundant in any season (Chace and Walsh 2006; Coogan etal. 2018;
Støstad etal. 2017). However, our results showed an increase in bird richness during the
rainy season. The rainy season coincides with the summer in Brazil, which is when many
T.Bhakti et al.
1 3
migrant species arrive in the region for reproduction, such as Cyclarhis gujanensis and
Ammodramus humeralis (Pinho etal. 2017; Somenzari etal. 2018), which could be respon-
sible for this result.
Insectivorous and omnivorous feeding preferences were the most common among bird
species in Ouro Preto. This result does not corroborate other studies that found insectivo-
rous species to be rare in urban centers (Sengupta etal. 2014; Seress and Liker 2015).
Insectivores are the most common birds in lists made in tropical natural areas due to their
use of different habitats and vegetation strata, ranging from understory birds to those liv-
ing in open areas (Anjos 2002; Hayes etal. 2020). The presence of many shrub and tree
patches in the urban center of Ouro Preto seems to facilitate the occurrence of insectivo-
rous species, probably due to available food and microhabitats, which reinforces the impor-
tance of maintaining such green areas in the urban matrix. Granivorous species, which,
due to their ample feeding, persist more easily in urban areas, were also widely observed.
Frugivores are more limited in terms of food and can thus experience local reductions
(Cleary etal. 2007; Gray etal. 2007; Kennedy etal. 2010), although the landscape of Ouro
Preto, due mainly to the presence of backyards with orchards, allows the existence of this
guild of birds. Granivores were associated mainly with open areas and, thus, were favored
by the large amount of herbaceous vegetation. These results are indicative of the heteroge-
neity of the landscape, which allows the occurrence of a wide variety of species of different
feeding guilds.
Finally, it is important to remember that this study was conducted in only one historic
city of Brazil and that the results need to be carefully considered, avoiding generalization.
Thus, the topics in the conclusion should be linked to the results found in the present study,
although suggesting a wide application. Further studies should be conducted in other his-
toric cities to assess whether the results presented in this study are repeated, increasing the
evidence of the importance of historic centers in maintaining a high diversity of birds in
cities.
5 Conclusion
Historical areas within cities are important for the conservation of bird species since
the lack of changes to them maintains, over time, small areas of vegetation that can
provide shelter and food for birds or function as stepping stones to larger forested areas
present in the vicinity.
Small green areas in historic cities can be relevant to the permeability of the urban
matrix for local biodiversity, especially when they provide heterogeneous environ-
ments.
Preserving the structure of ground cover not only leads to the protection of green areas,
but also favors the long-term maintenance of urban avifauna, including trophic guilds
that are not common in urban areas.
Acknowledgements Authors would like to thank the staff of the transport section of the Federal University
of Ouro Preto, Capes-Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for POM scholarship,
and RJY for English revision of the manuscript.
Author contributions CSA and POM conceived the project, designed research, and revised the manuscript.
POM, EFA, and FR collected and analyzed data. CSA, TB, and MAGF analyzed data and drafted the
manuscript.