Urban Forestry & Urban Greening 64 (2021) 127243

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Urban Forestry & Urban Greening

journal homepage: www.elsevier.com/locate/ufug

Bird species richness across a Northern Andean city: Effects of size, shape,
land cover, and vegetation of urban green spaces
Jaime A. Garizábal-Carmona a, b, *, N. Javier Mancera-Rodríguez a
a
Departamento de Ciencias Forestales, Grupo de Investigación Ecología y Conservación de Fauna Silvestre, Universidad Nacional de Colombia. Carrera 65 # 59A - 110,
Bloque 20, Oficina 211, Medellín, 050034, Colombia
b
Corporación Merceditas. Calle 3 29A-11, Casa 110, Medellín, 050021, Colombia

A R T I C L E I N F O A B S T R A C T

Handling Editor: Richard Hauer Cities are human-dominated ecosystems where landscape transformation decreases biodiversity, a conservation
concern when urbanization sprawls into biodiversity hotspots with high endemism. We aimed to evaluate the
Keywords: effects of site-specific features such as size and shape of green spaces, land cover, and vegetation on bird species
Introduced vegetation richness in Medellín, Colombia, a city of Northern Andes (n = 44 urban green spaces sampled from February
Tropical Andes
2018 to February 2019). We found 255 plant species: 23 % of trees and 41 % of understory were native sensu
Urban biodiversity
stricto (local origin); most native species and individuals were in green spaces lacking vegetation management.
Urbanization
Vegetation management Bird species richness (25.80 ± 8.05 resident species per sampling point; 83 resident species overall) increased
towards larger and more regular-shaped urban green spaces (squared or rounded), with less percentage of
impervious surfaces and more of grass–shrubs, and less influence of introduced trees in habitat structure (i.e. less
crown coverage, basal area, and average height). Bird species richness also increased when richness or abun­
dance of native understory vegetation sensu lato (local or regional origin) increased, but introduced trees
dominance represented higher and most significant effects to explain bird species richness. Increasing edge ef­
fects across urban green spaces and human-related habitat transformation favoring non-native vegetation might
represent significant constraints for enhancing local biodiversity in highly developed Andean cities.

1. Introduction ecological studies, as responses to urbanization depend on city charac­

Cities reflect modern human life and its impacts on the planet. Be­
sides topography and climate, human dynamics influence the compo­
sition and structure of cities, where natural landscapes are transformed
into novel ecosystems with reduced and structurally simple green spaces
(Aronson et al., 2017; Paz Silva et al., 2015; Shih, 2018). Non-native
introduced vegetation dominates urban green spaces (Nielsen et al.,
2013), which are mainly managed to improve public health and social
interaction (Dooling et al., 2006; McDonnell, 2011; Wolch et al., 2014).
Although some bird species benefit from non-native vegetation in cities
that offer novel resources (Chace and Walsh, 2006; Jasmani et al.,
2017), planted or naturalized vegetation has limited contribution in
maintaining local biodiversity (Aronson et al., 2017; Chong et al., 2014).
Recent thinking in urban planning includes biodiversity conserva­
tion as a key factor to make cities sustainable (Botzat et al., 2016;
Puppim De Oliveira et al., 2011; Threlfall and Kendal, 2018), but
decision-makers might fail to implement better practices without
teristics and surrounding landscape (Aronson et al., 2014; Kowarik,
2011; Mcdonald et al., 2009). This is particularly challenging when
cities are located in biodiversity hotspots with high endemism and
species turnover such as the Tropical Andes (Cincotta et al., 2000;
Rahbek et al., 2019), where urban bird studies are mainly species lists
that have limited use in biodiversity conservation (Ortega-Álvarez and
Macgregor-Fors, 2011).
Birds are well-known bioindicators in urban ecosystems (Mac­
gregor-Fors et al., 2015; Marzluff et al., 2001; Mckinney, 2008) as alpha
biodiversity measurements like species richness respond to green space
features at local scales (Marzluff et al., 2001; Mckinney, 2008; Tryja­
nowski et al., 2017): larger and more regular-shaped urban green spaces
(e.g. squared, rounded) are richer because they promote species
persistence due to species–area relationships (Beninde et al., 2015;
Fernández-Juricic and Jokimäki, 2001; Nielsen et al., 2013); they also
mitigate urban environmental pressures and edge effects (Fernández-­
Juricic, 2004), whereas smaller and less regular-shaped green spaces

* Corresponding author at: Cra. 77B #47 -70, 401, Medellín, 050031, Colombia.
E-mail addresses: jgarizabal@unal.edu.co (J.A. Garizábal-Carmona), njmancer@unal.edu.co (N.J. Mancera-Rodríguez).

https://doi.org/10.1016/j.ufug.2021.127243
Received 15 June 2020; Received in revised form 1 July 2021; Accepted 2 July 2021
Available online 6 July 2021
1618-8667/© 2021 Elsevier GmbH. All rights reserved.
J.A. Garizábal-Carmona and N.J. Mancera-Rodríguez
may act as ecological traps for most sensitive taxa (Lepczyk et al., 2017),
increasing risks of local extinction that reduce bird species richness.
The problem in highly developed Latin American cities is that green
spaces are surrounded by impervious surfaces, making it difficult to
manage the area and shape features of individual green spaces (Leveau
et al., 2017; Ortega-Álvarez and MacGregor-Fors, 2009; Paz Silva et al.,
2015). Therefore, most populated cities in the Northern Andes focus
urban planning on ecological connectivity frameworks to mitigate the
effect of habitat loss and fragmentation (Andrade et al., 2013), but local
governments also might enhance plant richness and abundance to in­
crease vegetation complexity structure, which is supposed to promote
habitat heterogeneity and local biodiversity (Collas et al., 2017; Roy
et al., 2012).
Managing site-specific features related to vegetation is an effective
alternative to promote local biodiversity in small green spaces
(Fernández-Juricic and Jokimäki, 2001; Morelli et al., 2017). Enhancing
tree or understory species richness might increase bird species richness
(Ferenc et al., 2014; Nielsen et al., 2013; Paker et al., 2014), as well as
habitat heterogeneity, especially when this is driven by native vegeta­
tion and natural regeneration (Chace and Walsh, 2006; Fontana et al.,
2011; Matthies et al., 2017; Threlfall et al., 2017; Yang et al., 2015).
Thus, less human-managed urban green spaces resembling natural
habitats of city surroundings usually increase local bird species richness
via colonization of less tolerant species to urbanization (Callaghan et al.,
2019; Fernández-Juricic, 2004; Marzluff, 2005).
Here, we present one of the first studies that evaluate effects of site-
specific features on local bird diversity (response variable) in urban
ecosystems of the Northern Andes, a region with growing urban­
ization–biodiversity conflicts (Bax and Francesconi, 2019). We per­
formed an exploratory analysis expecting that, besides area and shape
features, urban green spaces dominated by native understory and native
tree species would increase bird species richness. We focused on a
response variable and several predictors that could be easily accessible
Fig. 1. Study area and location of the 44 sampling points in western center Medellín, Colombia, Northern South America.
2
Urban Forestry & Urban Greening 64 (2021) 127243
to urban planners, and thus, prone to be included in green space local
management and biodiversity monitoring.
2. Methods
2.1. Study area
The municipality of Medellín is located along the Aburrá Valley in
Colombian Central Andes (6◦ 15′ N, 75◦ 34′ W; Fig. 1), in the Tropical
Andes biodiversity hotspot (Myers et al., 2000): 445 bird species and
2603 vascular plant species have been reported in the municipality
between ca. 1450 and 3000 m a. s. l. (Alcaldía de Medellín, 2015). This
hotspot with a high level of endemism is driven by the Andean uplift and
the derived biogeographical complexity of Northwestern South America
(Brumfield and Capparella, 1996; Rahbek et al., 2019).
Medellín belongs to a ten-municipality metropolitan area with
almost four million inhabitants living between 1450 and 1700 m a. s. l.
(Schnitter et al., 2006), where mean annual precipitations and temper­
atures range between ca. 1263–1920 mm and 15–20 ◦ C, respectively
(data taken from http://www.antioquiadatos.gov.co/). To evaluate sites
with similar environmental and urbanization pressures, with urban
green spaces of similar age but different size, shape, vegetation, and
management, we delimited an area of 1383 ha using a Digital Elevation
Model (DEM) and the GRASS GIS r.fill.dir tool to correct DEM imper­
fections (GRASS-Development-Team, 2017), interpolating with Delau­
nay triangulation method and processing outputs with r.watershed and
half–basin tools in the software QGIS (Quantum-GIS-Deve­
lopment-Team, 2018) (Fig. 1).
2.2. Sampling design
As we aimed to evaluate site-specific features on bird species rich­
ness, we considered sampling points rather than green spaces as the
J.A. Garizábal-Carmona and N.J. Mancera-Rodríguez
sampling units, establishing 200 m as the site-specific scale under
evaluation (e.g. Chong et al., 2014; Ferenc et al., 2014) and using a
systematic sampling design to locate sampling points in green spaces
>0.1 ha across a landscape dominated by impervious surfaces. We
located 44 sampling points, with 395 m being the mean closest distance
between points (min 200 m) (Fig. 1): six in three green spaces of ≥10 ha
with ≤10 % impervious cover (two non–urbanized plots and one pro­
tected urban reserve), two in green spaces ≥10 ha and >10 % imper­
vious cover (two university campuses), and 36 in green spaces ≤10 ha
(small parks, and street or stream green spaces). We distinguished
human-managed green spaces when found signals such as tree or shrub
pruning, or presence of turf grass lawns.
2.3. Urban green spaces structural and land cover features
We delimited green spaces based on satellite imagery with 10 m of
spectral resolution taken on 22 February 2019 by Sentinel-2 (USGS
EROS Archive), using streets and other continuous impervious surfaces
(sampling points located in the same green space shared values of area
and perimeter/area ratio). We estimated area and perimeter/area ratio
of each green space, and land cover type percentage for each sampling
point at 200 m radius from their centroids: grass–shrubs (without trees
above), trees (with or without understory underneath, as we could not
differentiate understory level when trees formed a continuous canopy),
and impervious surfaces (including buildings, roads, sidewalks, and
other surfaces without vegetation), based on the Tasseled cap trans­
formation index, a supervised coverage rating that classifies land
coverage types from satellite data using a mix of spectral indicators
(Samarawickrama et al., 2017); in our case, bands on brightness,
greenness, and wetness, assessing the procedure in the software QGIS
(Quantum-GIS-Development-Team, 2018). As data were not normally
distributed, which we evaluated with Shapiro-Wilk Normality Test using
the function shapiro.test of the package “stats” in R (R Core Team, 2019),
we performed Kruskal–Wallis and Wilcoxon rank sum pairwise tests
using the functions kruskal.test and pairwise.wilcox.test, respectively, of
the same R package, to evaluate differences between land coverage
types across the sampling points.
2.4. Vegetation surveys and species origin
We sampled plants from November 2018 to February 2019. For each
sampling point, we counted and identified all individuals of vascular
plants with circumference ≥10 cm at 130 cm high, hereafter “trees”, at
25 m radius circular plots (n = 44). We also counted and identified all
individuals with <10 cm at 130 cm high, hereafter “understory”, at five
2.5 m radius subplots per sampling point (220 subplots within the 44
main plots: one in the center of the main plot and four additional ones in
the midpoints towards each cardinal direction). In trees, we estimated
richness (number of species), abundance (number of individuals),
average height, basal area (from diameter at breast height; accuracy:
±0.01 m), and crown coverage (from two length measurements of tree
crown at 90◦ angle; accuracy: ±1.0 m). In understory, we estimated
richness and abundance per sampling point. For unidentified plants in
the field, we collected specimens to be identified at the University of
Antioquia Herbarium (HUA).
To assign species geographic distribution, we used local plant
checklists (Ortiz et al., 2019), and when information was ambiguous, we
asked up to six local experienced botanists for validation. We assigned
“introduced” for non–Neotropical species, “regional” for Neotropical
species distributed under 1000 m a.s.l., and “local” for species that
naturally occur within the Aburrá Valley above 1000 m a.s.l. To avoid
species recounting regarding their origin, we excluded dead trees, in­
dividuals identified only until family, and individuals identified only
until genus when more species of the same genus were present. We
performed Kruskal–Wallis and Wilcoxon rank sum pairwise tests (data
were not normally distributed) to evaluate differences between richness
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Urban Forestry & Urban Greening 64 (2021) 127243
and abundance of trees and understory across sampling points, consid­
ering their geographic distribution. Finally, we performed Man­
n–Whitney tests (data were normally distributed) to evaluate whether
human-managed green spaces had lower richness or abundance of
regional and local vegetation (both in trees and understory), which
might reflect some consequences of vegetation management and silvi­
cultural practices in the city.
2.5. Bird surveys
We sampled birds within 25 m fixed-radius points (n = 44) during
two seasons in 2018: five visits in February–April and five visits in
June–September (ten visits per point overall). We made bird surveys
only during favorable weather conditions (no rain, especially), adapting
protocols from Bibby et al. (1998), between 06:00 and 10:00 h, always
with the same observer (JAG) recording every individual seen or heard
in ten 10-minute visits per point (4400 min total). We excluded migra­
tory species and overflying birds. Bird species richness was the sum of
unique resident bird species recorded along the bird survey (cumulative
richness per sampling point without recounting species).
2.6. Explanatory variables
We took into account features on area and perimeter/area ratio to
evaluate the effects of green spaces size and shape; percentage of trees,
grass–shrubs, and impervious surfaces to evaluate the effects of land
cover; species richness and abundance of trees and understory, differ­
entiating each feature by introduced, regional and local origin, to
evaluate the effects of habitat composition; and tree basal area, canopy
coverage, and average height, also differentiating each feature by origin,
to evaluate the effects of tree level habitat structure (Supplementary
Table 1, Supplementary Table 2, Supplementary Table 3).
To account for multicollinearity and reduce the number of explan­
atory variables without excluding any feature (i.e. by preselection pro­
cedures), we performed Principal Components Analysis (PCA) using the
function rda of the package “vegan” in R (Oksanen et al., 2019), based on
four data sets of related features: 1) size and shape of urban green
spaces, and land cover features, 2) tree structural features, 3) tree spe­
cies richness and abundance, and 4) understory species richness and
abundance. For each data set, we used site scores of the main PCA axes
accounting for most of variation as final explanatory variables (based on
broken stick plotting, including two or three axes adding at least 75 % of
cumulative explained proportion) (Supplementary Table 4) (see Ferenc
et al., 2014).
Additionally, we performed a Mantel test using the function mantel.
rtest of the package “ade4′′ (Dray and Dufour, 2007) and found some
spatial autocorrelation of bird species richness across the study area;
therefore, we included another explanatory variable: a
distance-weighted autocovariate as a function of neighbouring response
values (Dormann et al., 2007), weighting by inverse distance and 0.7
(700 m) as the average sampling point radius, which was the minimum
radius in 0.1 scale where every sampling point had at least one neighbor
(we started exploring with 100 m). We constructed this autocovariate
using the function autocov_dist of the package “spdep” (Bivand and Piras,
2015), using longitude and latitude of each sampling point as the matrix
of coordinates and bird species richness as the response variable.
2.7. Data analysis
In regards to the response variable (bird species richness), we eval­
uated completeness of bird census with coverage-based rarefaction/
extrapolation curves for diversity order q = 0: species richness with Hill
numbers (95 % confidence intervals and 500 bootstrap replications; data
type = abundance), using the package “iNEXT” in R (Hsieh et al., 2016).
In regards to the explanatory variables, we used the selected 11 PCA
axes and the spatial autocovariate (Supplementary Table 4), which were
J.A. Garizábal-Carmona and N.J. Mancera-Rodríguez Urban Forestry & Urban Greening 64 (2021) 127243

low correlated to each other when plotting a correlation matrix using the always higher than those of regional and local species (Table 1).
function chart.Correlation of the package “PerformanceAnalytics”, ran
with the Spearman correlation coefficient (Peterson et al., 2019) (Sup­ 3.2. Bird species composition and richness
plementary Fig. 1, Spearman correlation coefficients always <0.7 or
p-value >0.05). We also plotted correlation matrices with all selected We found 81 Neotropical and two non–Neotropical resident bird
PCA axes and the raw variables within each data set to facilitate further species (Supplementary Table 6), with overall sampling coverage above
interpretation of each feature effects on bird species richness (Supple­ 0.99 (all points merged) and usually above 0.70 per sampling point
mentary Fig. 2, Supplementary Fig. 3, Supplementary Fig. 4, Supple­ (evaluating each point independently), according to sample-size-based
mentary Fig. 5). and coverage-based rarefaction curves (Supplementary Fig. 6). We
We used the generalized linear models (GLM) approach, selecting the observed 25.80 (±8.05) resident bird species per point, with 10.57
best models using the function glmulti of the “glmulti” package (version (±3.72) species recorded per visit.
1.0.7.1.) in R (Calcagno and de Mazancourt, 2010), fitting all candidate
models under Poisson distribution, without redundant formulas
3.3. Bird species richness according to green spaces composition and
(method = “h”), ranking candidate models using the Akaike’s Infor­
structure
mation Criterion corrected for small sample sizes (AICc), and restricting
the best model’s selection to main effects. We presented and discussed
After comparing 8450 models, the best model we found (ΔAICc = 0)
models with ΔAICc ≤ 2.0; we checked overdispersion of models and
suggested that bird species richness increased significantly with the first
correlation between predictors by evaluating residual deviance and
PCA axis accounting for multicollinearity of size, perimeter/area ratio of
variance inflation factors (VIF), respectively: residual deviance lower
urban green spaces, and land cover features (PC1-Land: 61 % of variance
than degrees of freedom was considered low overdispersion and VIF ≤ 5
explained), and the first PCA axis accounting for multicollinearity of tree
using the vif function of the “car” package (Fox and Weisberg, 2019) was
structural features (PC1-TStr: 34 % of variance explained) (Table 2,
considered low correlation. Finally, we estimated each predictor’s esti­
Supplementary Fig. 1). The explanatory variable PC1-Land was strongly
mate, standard error, z–values, and each model weight (probability that
and negatively correlated (Spearman correlation coefficient >0.8, p-
each given model is the best model) using the function glm of the “stats”
value <0.001) with the perimeter/area ratio of urban green spaces and
package (R Core Team, 2019), and the adjusted coefficient of determi­
the percentage of impervious surfaces (Supplementary Fig. 2), and
nation (Adj–R2) using the rsq function of the “rsq” package (Zhang,
positively correlated with the size of urban green spaces and the per­
2020).
centage of grass–shrubs (Supplementary Fig. 2), which implies that
larger and more regular-shaped urban green spaces (squared or
3. Results
rounded) and sites with less impervious surfaces and more grass–shrubs
increased bird species richness. On the other hand, the explanatory
Urban green spaces ranged between 0.11 and 103.73 ha of size
variable PC1-TStr was strongly and positively correlated with crown
(9.44 ± 24.17 on average), and between 0.005 and 0.124 m− 1 of
coverage, basal area, and average height of introduced tree species
perimeter/area ratio (0.059 ± 0.029), across a landscape with signifi­
(Supplementary Fig. 3), which implies that increasing introduced tree
cant variation in percentage of trees, grass–shrubs, and impervious
structural dominance decreased bird species richness.
surfaces (Kruskal–Wallis test: F-value = 18.86, p-value <0.001). We
The best model also included the third PCA axis accounting for
found land cover differences particularly when comparing impervious
multicollinearity of understory richness and abundance (PC3-Und: 17 %
surfaces (44.31 % ±23.83) with trees (25.85 % ±14.69; Wilcoxon rank
of variance explained), which was positively correlated with regional
sum test: adjusted p-value <0.001) and grass–shrubs (29.83 % ±18.38;
Wilcoxon rank sum test: adjusted p-value = 0.002), with no significant
Table 1
differences between trees and grass–shrubs (Wilcoxon rank sum test:
Mean and standard deviation (SD) of evaluated vegetation features across 44
adjusted p-value = 0.46).
urban green spaces of Medellín, Colombia, Northern South America: richness
(species), abundance (individuals), basal area (m2), and crown coverage (m2),
3.1. Vegetation composition and structure differentiating totals and by species origin (introduced: non–Neotropical spe­
cies, regional: Neotropical species below 1000 m a.s.l., and local: native within
We found 2136 individuals of trees and 1196 individuals of under­ Aburrá Valley above 1000 m a.s.l.).
story, with 255 species overall: 205 of them found in trees and 98 in Vegetation Mean ± SD Vegetation Feature Mean ± SD
understory, and 48 species (18 %) shared between categories; 157 Feature
species were exclusive of trees (62 %) and 50 of understory (20 %) Introduced Introduced basal
(Supplementary Table 5). Introduced trees were more abundant and had richness area
more species richness than regional and local trees across urban green Trees 7.70 ± 3.61 Trees 239.43 ± 168.85
spaces (Kruskal–Wallis test: tree richness = 33.17, p-value <0.001; tree Understory 0.96 ± 1.16 Understory –
Regional richness Regional basal area
abundance = 38.34, p-value <0.001), whereas introduced understory
Trees 6.23 ± 4.06 Trees 89.59 ± 93.42
plants were more abundant (Kruskal–Wallis test: tree richness = 4.74, p- Understory 1.07 ± 1.02 Understory –
value = 0.01) but had similar species richness than regional and local Local richness Local basal area
understory plants (Kruskal–Wallis test: understory richness = 4.76, p- Trees 3.4 ± 3.2 Trees 63.3 ± 73.4
value = 0.09). Understory 1.6 ± 3.6 Understory –
Introduced Introduced crown coverage
Sites with less human-managed vegetation showed higher species abundance
richness of regional and local species at both trees and understory (all p- Trees 22.25 ± 10.45 Trees 1686.89 ± 1090.34
values in Mann–Whitney tests were <0.05), but these sites were rare in Understory 1.23 ± 1.70 Understory –
the study area (only nine of the 44 sampling points). On average, total Regional Regional crown
abundance coverage
tree and understory species richness decreased 46 % (±17) and 36 %
Trees 14.25 ± 16.77 Trees 968.09 ± 1203.06
(±38) per sampling point when we excluded introduced species, and 80 Understory 4.18 ± 7.25 Understory –
% (±18) and 80 % (±30) when we excluded both introduced and Local abundance Local crown
regional species (only local species left), respectively. We found similar coverage
decreases in abundance and tree structural features when species origin Trees 11.3 ± 22.5 Trees 494.0 ± 534.8
Understory 14.0 ± 34.9 Understory plants
was distinguished, with average values of introduced species being
–

4
J.A. Garizábal-Carmona and N.J. Mancera-Rodríguez Urban Forestry & Urban Greening 64 (2021) 127243

Table 2
Best supported models for evaluating local bird species richness (BR) across urban green spaces in the city of Medellín, Colombia, Northern South America (n = 44).
Models are compared using the Akaike Information Criterion corrected for small sample sizes (AICc) and only models with ΔAICc < 2.0 are shown with their weights
(W). Adjusted coefficient of determination (Adj-R2) of models are also shown. Significance of variables for each model are marked as ***: p < 0.001, **: p < 0.01, and
*: p < 0.05.
Model formula and variable significance Estimate SE z–value AICc ΔAICc W Adj–R2

BR ~ PC1-Land + PC1-TStr + PC3-Und 270.18 0.00 0.13 0.62

PC1-Land: size, shape, land cover*** 0.329 0.057 5.82
PC1-TStr: tree structural features** − 0.131 0.047 − 2.79
PC3-Und: understory richness–abundance 0.081 0.051 1.57
BR ~ PC1-Land + PC1-TStr 270.20 0.02 0.13 0.57
PC1-Land: size, shape, land cover*** 0.288 0.050 5.82
PC1-TStr: tree structural features** − 0.141 0.047 − 3.02
BR ~ PC1-Land + PC1-TStr + PC2-Tree + PC3-Und 270.34 0.16 0.12 0.62
PC1-Land: size, shape, land cover*** 0.3797 0.065 5.79
PC1-TStr: tree structural features* − 0.1132 0.048 − 2.37
PC2-Tree: tree richness–abundance 0.084 0.055 1.54
PC3-Und: understory richness–abundance 0.089 0.052 1.71
BR ~ PC1-Land + PC1-TStr + PC2-Tree 270.67 0.49 0.10 0.59
PC1-Land: size, shape, land cover*** 0.331 0.058 5.67
PC1-TStr: tree structural features* − 0.125 0.047 − 2.62
PC2-Tree: tree richness–abundance 0.076 0.054 1.39
BR ~ PC1-Land + PC1-TStr + PC2-TStr + PC2-Tree + PC3-Und 271.24 1.06 0.07 0.63
PC1-Land: size, shape, land cover*** 0.412 0.070 5.89
PC1-TStr: tree structural features* − 0.107 0.048 − 2.22
PC2-TStr: tree structural features 0.067 0.050 1.34
PC2-Tree: tree richness–abundance* 0.117 0.059 1.97
PC3-Und: understory richness–abundance 0.094 0.052 1.79
BR ~ 1 + PC1-Land + PC1-TStr + PC2-Und + PC3-Und 271.35 1.17 0.07 0.60
PC1-Land: size, shape, land cover*** 0.358 0.062 5.78
PC1-TStr: tree structural features** − 0.141 0.048 − 2.95
PC2-Und: understory richness–abundance 0.059 0.050 0.050
PC3-Und: understory richness–abundance 0.089 0.052 0.052
BR ~ 1 + PC1-Land + PC1-TStr + PC1-Und 271.62 1.44 0.06 0.58
PC1-Land: size, shape, land cover*** 0.322 0.065 3.795
PC1-TStr: tree structural features* − 0.123 0.050 − 2.474
PC1-Und: understory richness–abundance − 0.068 0.068 − 1.002
BR ~ PC1-Land + PC1-TStr + PC2-TStr + PC2-Tree 271.70 1.52 0.06 0.60
PC1-Land: size, shape, land cover*** 0.358 0.063 5.732
PC1-TStr: tree structural features* − 0.119 0.048 − 2.494
PC2-TStr: tree structural features 0.061 0.050 1.234
PC2-Tree: tree richness–abundance 0.105 0.059 1.782
BR ~ PC1-Land + PC1-TStr + PC2-Und 271.72 1.54 0.06 0.58
PC1-Land: size, shape, land cover*** 0.908 0.054 5.722
PC1-TStr: tree structural features** − 0.149 0.048 − 3.140
PC2-Und: understory richness–abundance 0.047 0.050 0.915
BR ~ PC1-Land + PC1-TStr + PC2-Tree + PC2-Und + PC3-Und 271.74 1.56 0.06 0.63
PC1-Land: size, shape, land cover*** 0.407 0.070 5.825
PC1-TStr: tree structural features* − 0.123 0.049 − 2.523
PC2-Tree: tree richness–abundance 0.083 0.055 1.516
PC2-Und: understory richness–abundance 0.057 0.049 1.146
PC3-Und: understory richness–abundance 0.097 0.052 1.850
BR ~ PC1-Land + PC1-TStr + PC3-TStr + PC3-Und 271.75 1.57 0.06 0.61
PC1-Land: size, shape, land cover*** 0.349 0.060 5.792
PC1-TStr: tree structural features** − 0.124 0.047 − 2.629
PC3-TStr: tree structural features 0.046 0.047 0.985
PC3-Und: understory richness–abundance 0.088 0.052 1.683
BR ~ PC1-Land + PC1-TStr + PC3-TStr 272.00 1.82 0.05 0.58
PC1-Land: size, shape, land cover*** 0.302 0.052 5.746
PC1-TStr: tree structural features** − 0.136 0.047 − 2.899
PC3-TStr: tree structural features 0.036 0.046 0.788

understory richness and abundance (Spearman correlation coefficient
<0.8, p-value <0.001, Supplementary Fig. 5); nevertheless, the variable
PC3-Und had no significant effect on bird species richness in any of the
best models (ΔAICc ≤2.0) (Table 2, Supplementary Fig. 1), whereas
PC1-Land and PC1-TStr were present and statistically significant in all of
them (p-value <0.05) (Table 2). Other PCA axes accounting for multi­
collinearity were included in some of the best models, but only the
second axis accounting for multicollinearity of tree richness and abun­
dance (PC2-Tree: 28 % of variance explained) had significant effects on
bird species richness (only in one model) (Table 2). The explanatory
variable PC2-Tree was negatively correlated with regional and local tree
richness and abundance (Supplementary Fig. 4) (Spearman correlation
coefficient <0.8, p-value >0.05), which implies that increasing regional
or local tree richness or abundance decreased bird species richness.
4. Discussion
Several studies have suggested that native vegetation can mitigate
the negative effects of urbanization on local bird diversity (e.g. Chace
and Walsh, 2006; Chong et al., 2014; Dale, 2018; Threlfall et al., 2017);
thus, although we expected that bird species richness would respond to
species–area relationships (Beninde et al., 2015; Fernández-Juricic and
Jokimäki, 2001; Nielsen et al., 2013), we also expected that it would
respond to richness or abundance of native trees and understory.
Nevertheless, we found that site-specific features such as size and
perimeter/area ratio of green spaces, as well as land cover and habitat

5
J.A. Garizábal-Carmona and N.J. Mancera-Rodríguez
types highly influenced by human disturbance, vegetation management
or silvicultural practices overcame the effects of features driven by
native understory and tree species.
In highly developed urban areas of Medellín (Colombia), bird species
richness increased towards larger and more regular-shaped urban green
spaces (squared or rounded), structural features constrained by green
spaces loss and fragmentation driven by urbanization (Fernández-Juri­
cic and Jokimäki, 2001; Kang et al., 2015; Kowarik, 2011; Shih, 2018;
Xie et al., 2016); also, it increased towards green spaces with lower
percentage of impervious surfaces and higher percentage of grass­
–shrubs, features constrained by urbanization sprawl and urban green
spaces management, respectively (Aronson et al., 2017; Fernández-­
Juricic and Jokimäki, 2001; Mckinney, 2008; Sushinsky et al., 2013). In
regards to vegetation, bird species richness increased towards green
spaces with lower introduced tree dominance (i.e. lower crown
coverage, basal area, and average height), which depends on reducing
silvicultural practices favoring introduced vegetation at tree level
(Aronson et al., 2017; Chong et al., 2014; Nowak, 2012; Quinton et al.,
2020). Besides, we found positive but no significant effects of richness or
abundance of native understory (both regional and local), and few evi­
dence supporting any effect of native trees (both regional and local).
Besides highlighting the relative effects of each feature on bird spe­
cies richness, enhancing bird diversity would rely on understanding
what features are easier to manage and how urban planning might
improve their strategies for optimizing green spaces in highly developed
urban matrices. In areas dominated by isolated and relatively small
green spaces (median ~ 1 ha in our case), reducing edge effects could be
a key factor to enhance local bird diversity (Fernández-Juricic and
Jokimäki, 2001; Ives et al., 2011; Johnson and Karels, 2016; M. Zhang
et al., 2018). Some studies in highly developed cities suggest that
perimeter/area ratio or related shape indicators are better predictors of
local bird diversity than size of urban green spaces (Horák, 2016; Shih,
2018). Nevertheless, although improving shape features of green spaces
(i.e. more regular shapes) could be easier than increasing their size, any
feature that need space for biodiversity conservation in highly devel­
oped cities is hard to manage, especially in Latin America where social
and economic factors still represent the cornerstone of urban planning
and urban development policies (CAF, 2017).
Under such a scenario where landscape physical constraints on green
spaces such as size, shape, and connectivity networks between green
spaces increase edge effects (Beninde et al., 2015; Fernández-Juricic and
Jokimäki, 2001; Najihah et al., 2017), and habitat transformation driven
by urbanization reduces suitable habitat for urban avoider bird species
(Blair, 1996; Chace and Walsh, 2006), increasing trees and understory
richness or volume could be an alternative strategy to improve urban
green spaces functionality (Müller et al., 2018; Threlfall et al., 2017);
nevertheless, vegetation could have different effects on bird commu­
nities according to the proportion of native plant species.
We found mainly negative effects of trees on bird species richness,
regarding both land cover (i.e. trees) and tree level features, due to the
high dominance of introduced species that reduces habitat heterogene­
ity and the influence of native trees (González-Oreja et al., 2012; Jas­
mani et al., 2017; Paz Silva et al., 2015). On the other hand, we found
mainly positive effects of understory regarding both land cover (i.e.
grass–shrubs) and understory level features, due to the incidence of
native vegetation that increases the availability of refuges, preys, and
nesting sites for less tolerant bird species to urbanization, most of them
related to understory vegetation (Matsuba et al., 2016; Rousseau et al.,
2015; G. Yang et al., 2015).
Other studies have suggested positive effects of trees on bird species
richness when urban plant communities are dominated by native species
(i.e. higher percentage of native trees in urban green spaces) (Barbosa de
Toledo et al., 2012; de Castro Pena et al., 2017; Le Roux et al., 2018),
and negative effects of understory when vegetation is dominated by
non-native ornamental plants (Aronson et al., 2014; Wang et al., 2017);
so that, as Andean native forests with their native plants have almost
6
Urban Forestry & Urban Greening 64 (2021) 127243
disappeared from the city (Molina-Franco, 2015; Quintero et al., 2017),
improving local management practices on green spaces in Medellín and
similar Andean cities could be a key factor for enhancing local biodi­
versity under the dynamics of a novel ecosystem (Fontana et al., 2011;
Kowarik, 2011; Shwartz et al., 2013).
We found higher bird species richness in less human-managed sites
(with more regional or local understory and less dominance of intro­
duced trees), evidencing that some silvicultural practices and vegetation
management could have little effects or even negative effects on urban
bird biodiversity (Aronson et al., 2014; Kowarik, 2011; Mckinney, 2008;
Pauchard et al., 2006). In addition, only one of the green spaces that we
found with higher bird species richness is recognized as an important
area for bird diversity conservation in the city (“Cerro El Volador”)
(Vásquez-Muñoz and Castaño-Villa, 2008), with the others representing
non-urbanized plots with no public or private protection. Indeed, after
our sampling exercise in 2018–2019, at least two of these unprotected
green spaces have been already urbanized, replacing previous vegeta­
tion by impervious surfaces and managed green spaces, which accord­
ingly to our findings, probably reduced local bird species richness.
Increasing introduced tree or understory vegetation is a direct
consequence of silvicultural practices following ornamental rather than
ecological criteria (Dooling et al., 2006; McDonnell, 2011; Pauchard
et al., 2006), whereas increasing native tree or understory vegetation
usually rely on less human management and less influence of silvicul­
tural practices (Aronson et al., 2014; Threlfall et al., 2017). Therefore, it
seems that an effective way to increase local biodiversity in highly
developed cities with space limitations is to discourage human distur­
bance on vegetation (Fernández-Juricic, 2004; Kang et al., 2015; Müller
et al., 2018) and include denser native understory vegetation in existing
urban green spaces (Aronson et al., 2014; Jasmani et al., 2017; Paker
et al., 2014; Threlfall et al., 2017). Nevertheless, this represents other
challenges such as social aesthetic perception and citizen security
(Carrus et al., 2015; Soga et al., 2016; Yang et al., 2019).
Finally, it might be relevant to evaluate in more detail bird species
composition and species-specific responses to urbanization at both local
and regional scales, as different elements of urban environments support
different components of biodiversity (Morelli et al., 2017), and bird
species respond in different ways to urbanization regarding their
biogeographic origin (González-Oreja, 2011). Fortunately, there are still
many unveiled biodiversity patterns and drivers to investigate in Trop­
ical Andes (MacGregor-Fors and Ortega-Álvarez, 2013; Marzluff, 2017;
Ortega-Álvarez and Macgregor-Fors, 2011); unfortunately, urbanization
trend to homogenize bird communities (Leveau et al., 2017; McKinney,
2006) might obscure some of them, while urbanization growing rate
across this biodiversity hotspot with high endemism and species turn­
over is probably higher than the growing rate of research.
5. Conclusions
In a highly developed Andean city, features that best explained bird
species richness across urban green spaces were size and shape of urban
green spaces, percentage of impervious surfaces and grass–shrubs
(artificial coverage and incipient natural regeneration, respectively),
and dominance of introduced trees in habitat structure. The effect of
features such as species richness or abundance of native trees and un­
derstory had lower effects on bird species richness, mainly due to their
low representativity in urban green spaces, especially at tree level.
Our results suggest that a key point for enhancing urban local bird
richness could be decreasing the proportion of introduced trees and
promoting a higher prevalence of native understory vegetation. Man­
aging perimeter/area ratio of urban green spaces seems less practical
and increasing their size less relevant as area thresholds < 3.0 ha have
been suggested for increasing bird species richness within urban eco­
systems (Chang and Lee, 2016; Morelli et al., 2018). In other words,
relatively small areas could improve functionality for increasing local
bird diversity under better management on vegetation composition and
J.A. Garizábal-Carmona and N.J. Mancera-Rodríguez
structure.
Hence, in the matter of urban planning, the more plant species and
the larger urban green spaces are not necessarily the better or the easier:
it depends on how urban green spaces composition and structure are
aligned with local biodiversity, along with the conservation possibilities
under the specific urbanization scenario.
CRediT authorship contribution statement
Jaime A. Garizábal-Carmona: Conceptualization, Sampling design,
Data acquisition- Curation- Analysis, Data interpretation, Writing-
Original draft preparation, Visualization, Investigation. N. J Mancera-
Rodríguez: Supervision, Validation, Writing- Reviewing and Editing
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
We thank the University of Antioquia Herbarium (HUA) and all their
staff, especially Wilson Renfijo, Ricardo Callejas, Felipe Cardona, Álvaro
Roldán, and Heriberto David. We also thank Paula Morales, Tomás
Hinestroza, Samuel Monsalve, Andrés Mercado, Deysi Carmona, Wilson
Rodríguez, Manuel Bernal, and Luisa Arboleda for supporting vegetation
assessments, Natalia Ruiz and Luz Morales for GIS support, Victor
Martínez-Arias for statistical support. We thank Benjamin Low and
Amanda Colón for language editing, and Christopher Lepczyk, Viviana
Márquez and two anonymous reviewers for comments that help to
improving the final version of the manuscript.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.ufug.2021.127243.
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