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Bird community responses to different urban conditions in La Paz, Bolivia

Article in Urban Ecosystems · September 2010

DOI: 10.1007/s11252-010-0126-7

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Urban Ecosyst (2010) 13:375–391
DOI 10.1007/s11252-010-0126-7

Bird community responses to different urban conditions

in La Paz, Bolivia

Mariana Villegas & Álvaro Garitano-Zavala

Published online: 21 April 2010

# Springer Science+Business Media, LLC 2010

Abstract Urbanization alters ecosystems worldwide, but little is known about its effects in
the Neotropical region. In the present research we examined the relative influence of
different levels of urbanization and of some urban development measures on bird species
richness, abundance and composition. We surveyed 104 observation stations at which we
collected data on the relative abundance of bird species, and also data on seven
environmental variables as measures of urban development and human activity. We
registered 57 native bird species. Bird species richness and bird abundance increased with
lower urbanization levels. Both variables were positively related to vegetation cover and
native vegetation, and negatively to built-up cover, abundance of Rock Pigeon (Columa
livia), pedestrian rate and car rate. A canonical correspondence analysis produced a
significant model that explained 37% of the total variation in species data. This analysis
segregated bird species along two important gradients: urbanization and elevation. The
most urbanized areas were dominated by a few synanthropic species tolerant to human
disturbance, such as Rufous-Collared Sparrow (Zonotrichia capensis), Eared Dove
(Zenaida auriculata) or Chiguanco Thrush (Turdus chiguanco). Areas with lower
urbanization levels had more species typically associated with native vegetation, such as
Plain-Mantled Tit-Spinetail (Leptasthenura aegitaloides) or D’Orbigny’s Chat-Tyrant
(Ochthoeca oenanthoides), among others. Elevation had a significant influence in
structuring bird communities, with some species restricted to higher elevations and some
to lower elevations. Although changes in elevation had an important influence, urbanization

M. Villegas (*)
Carrera de Biología, Universidad Mayor de San Andrés, Casilla 10077( La Paz, Bolivia
e-mail: mariana.villegas@gmail.com

Á. Garitano-Zavala
Unidad de Manejo y Conservación de Fauna, Instituto de Ecología, Carrera de Biología,
Universidad Mayor de San Andrés, Casilla 10077( La Paz, Bolivia

Present Address:
M. Villegas
Department of Biology, University of Missouri—St. Louis, One University Boulevard
St. Louis, MO 63121, USA
376 Urban Ecosyst (2010) 13:375–391

had a stronger effect on structuring bird communities. This study provides valuable
information and an important baseline for future studies.

Keywords Andes . Bird communities . Elevation . Gradient . Urban ecology . Urbanization

Introduction

Urban ecosystems are emergent phenomena in which humans are a dominant component
(Alberti et al. 2003). As in other ecosystems, the processes that take place within them are a
result of their interacting constituents (Alberti et al. 2003); however, these processes
encompass several irreversible and persistent changes through growth of human
populations and land transformation, among others (Vitousek et al. 1997). Historically,
conservation has tended to focus on lands with small human presence (Miller and Hobbs
2002), but cities are growing rapidly worldwide and it has become imperative to study and
understand the ecological processes within these ecosystems. Urban ecology needs to be
addressed along with other aspects of conservation and urban planning (Niemelä 1999;
Marzluff and Ewing 2001; Alberti et al. 2003).
Urbanization is a continuous process that produces a range of settlement densities and
patterns (Marzluff et al. 2001) characterized by concentrated human presence (Chace and
Walsh 2004) that significantly influence the functioning of local and global ecosystems
(Vitousek et al. 1997; Grimm et al. 2000; Alberti 2005). Replacement of vegetation by
impervious surfaces reduces the number of species and alters resident animal communities
(Hansen et al. 2005; McKinney 2008). Numerous studies have evaluated effects of
urbanization on birds, and most of them have found that birds are negatively affected by
urbanization and its associated processes (Clergeau et al. 1998; Fernández-Juricic and
Jokimäki 2001; Marzluff et al. 2001; McKinney 2002, 2008; Alberti et al. 2003; Melles et
al. 2003; Blair 2004; Donnelly and Marzluff 2006; Schlesinger et al. 2008). Urbanization
not only reduces bird richness (Beissinger and Osborne 1982; Marzluff et al. 2001;
McKinney 2002) but also alters the composition of bird communities by increasing the
fitness of synanthropic species (associated with humans) and decreasing the fitness of
species associated with native habitat (Donnelly and Marzluff 2006).
Several studies have shown that it is important to consider features of the surrounding
landscape when examining habitat use by birds (Miller et al. 2003). To describe and
quantify the degree of urbanization, many studies have used measures such as percentage of
vegetation cover, distance to urban core (McDonnell et al. 1997) or density of houses
surrounding the area, among others (Marzluff et al. 2001). At local scales, some measures
may also be considered such as human presence and activity (Schlesinger et al. 2008);
human presence (e.g. pedestrian rate), for example, reduces richness and abundance of birds
(Fernández-Juricic 2000). Habitat and environmental characteristics such as these can have
great influence in structuring bird communities (Clergeau et al. 1998; Fernández-Juricic and
Jokimäki 2001).
Although cities of the Neotropical region are growing extremely fast and will continue to
grow (United Nations Population Fund 2007), very little is known about the effects of
urbanization on bird communities in these areas (Marzluff et al. 2001). Many of the studies
conducted in Latin America have shown that bird species richness declines with increasing
levels of urban development (Reynaud and Thioulouse 2000; Díaz and Armesto 2003;
Leveau and Leveau 2004; Ortega-Álvarez and MacGregor-Fors 2009) and also that
urbanization leads to the dominance of a few successful species that benefit from human
Urban Ecosyst (2010) 13:375–391 377

resources (Leveau and Leveau 2005; Ortega-Álvarez and MacGregor-Fors 2009). Several
other studies have evaluated trophic composition of bird communities in urban areas
(Mendonça-Krügel and dos Anjos 2000; Manhães and Loures-Ribeiro 2005; MacGregor-
Fors 2008; Muñoz et al. 2007) and have found that omnivores and granivores are more
common in areas with higher urban development, whereas frugivores and nectarivores
increase with decreasing urbanization.
The city of La Paz, Bolivia, had an accelerated growth during the twentieth century,
largely a consequence of migration from rural areas (Villagómez 1991). To date, two
studies have addressed the influence of urbanization on birds in La Paz (Garitano-Zavala
and Gismondi 2003; Villegas and Garitano-Zavala 2008). The first study examined bird
species richness and diversity in parks in relation to total area, vegetation cover and
abundance of Rock Pigeon (Columba livia), and the second study proposed the selection of
groups of species as indicators of human impact. Given the rapid growth of human
population and urban development, understanding and recognizing the outcomes of
urbanization on ecological processes, may assist in conservation of bird communities in this
urban landscape, and also may provide city authorities with tools for urban planning.
Our main objective was to contribute to a better knowledge of bird communities in La
Paz, and to describe to some extent how they are affected by urbanization. We address the
following questions: a) How are bird species richness and abundance influenced by
different local habitat and urban development measures, and by different levels of
urbanization?; b) How do these measures influence species composition?; and c) How
much of the variation in species composition can be explained by these measures? For the
first question, we predict that species richness and abundance will decline with increasing
levels of urban development. For the second question, we predict that few bird species will
be found in highly urbanized environments, compared to higher number of species in
environments with low levels of urbanization. We expect the habitat and urban
development measures to explain high percentages of variation in species composition.

Methods

Study area

La Paz is located in the Central Andes in the valley of La Paz river, east of the Andean high
plateau, at the base of the Cordillera Oriental (Baudoin 1991; Liberman 1991). It extends
along an elevational gradient from 2,700 to 4,100 m, covering an area of approximately
186 km2 (RED Habitat 2004). The city had an accelerated growth over the last century
mainly due to migration from rural areas (Villagómez 1991); that growth has been covering
available land areas, slopes and hillsides on higher elevations. It has a human population of
more than a million inhabitants (RED Habitat 2004). The annual rate of population increase
estimated for Bolivia is 1.38% (INE 2006), but the rate can vary within urban or rural areas.
The settled area of La Paz is distributed according to topography and spatial characteristics;
it is mainly established at mid-elevations (around 3,600 m) and along the radial river
valleys and canyons which resemble branches. Urban and commercial areas (areas with
high density of multi-storied buildings for commerce, service and industry) are located
northwest of the city (between 3,500 and 3,800 m elevation); suburban areas (characterized
by moderate to high-density housing with lawns and gardens) are mostly at lower
elevations south of the city; and exurban areas (with individual homesteads and recreational
developments surrounded by natural matrix) and rural areas (individual homesteads
378 Urban Ecosyst (2010) 13:375–391

surrounded by agricultural matrix) are scattered along the periphery of the city, throughout
the elevational gradient. Definitions of urban, suburban, exurban and rural areas follow
Marzluff et al. (2001).
Vegetation within the city is highly impoverished. Originally the region was covered
with Polylepis forest, together with different species of shrubs and bushes such as Dunalia
brachyacantha, Psoralea pubescens and Achyrocline satureoides, among others (Navarro
and Maldonado 2002). Dry forest species, such as Prosopis laevigata, Caesalpinia bangii
or Tecoma arequipensis, likely occurred in lower elevations (Navarro and Maldonado
2002). At present, within the city the native shrub stratum has second-growth species such
as Viguiera pazensis, Nicotiana glauca, Malva parviflora, Mutisia acuminata, Adesmia
miraflorensis, Baccharis spp. and Cortaderia spp.; the arboreal stratum is mainly
represented by exotic species such as Eucalyptus globulus, Cupressus macrocarpa, Acacia
retinoides, A. dealbata, Pinus radiata, Populus nigra and P. balsamifera (García 1991).

Avian surveys

We collected data on the relative abundance of bird species at 104 observation stations
randomly distributed over La Paz (Fig. 1). To select those stations, we placed an imaginary
grid of one hectare-cells over a map of the city (obtaining 24,528 cells). This one hectare-
cell size was chosen because it represents the average size of a block in La Paz. We
randomly selected 104 cells and established an observation station at the center of each cell.

Fig. 1 Location of observation stations in La Paz

Urban Ecosyst (2010) 13:375–391 379

If the observation station was located within private property or was inaccessible because of
topography, we slightly moved the observation station within the cell trying to get as much
visibility as we could. The selected observation stations had a minimum distance of 250 m
from each other (Ralph et al. 1995). We surveyed birds at each station between 6:30 and
10:30, using fixed-radius (50 m) point counts, during which we recorded the species and
number of all native birds seen within 15-min sampling periods (Ralph et al. 1995). We
performed three counts at each observation station between September 2004 and February
2005. To the extent possible, the three counts were evenly spread throughout the 6-month
sampling period, and spread during morning hours to ensure that each station was surveyed
throughout the 4-hour sampling period. All the surveys were conducted by one of the
authors (MV).

Urban characterization

In order to describe the local habitat, urban development and human activity, in each
observation station we registered seven environmental variables: a) Elevation: measured
with altimeter/barometer KONUS®; b) Built-up cover: visually estimated and expressed in
percentage, it is the land surface within one hectare from the center of the point-count,
covered by houses, buildings, concrete, asphalt or any other construction material; c)
Vegetation cover: also visually estimated and expressed in percentage, it is the land surface
within one hectare from the center of the point-count, covered by all kinds of herbaceous,
arboreal or shrubby vegetation; d) Native vegetation: proportion of native vegetation,
visually estimated and expressed in percentage; e) Pedestrian rate: we conducted counts
during the second and third avian surveys, in which we counted the pedestrians passing by
or standing in two 10-min periods; the obtained values were averaged to get one final value
of pedestrians per minute per station; f) Car rate: following the same method used for
pedestrian rate, we conducted counts of the cars passing by during two 10-min periods, and
obtained one value of cars per minute per station; and g) Abundance of Rock Pigeon
(Columba livia) (hereafter abundance of C. livia): regarded as the maximum number of
individuals recorded at an observation station, during the bird surveys. All these measures
were recorded within one hectare, considering the point-count as the center of the hectare.
Abundance of C. livia was used as a variable to describe the local habitat and urban
development because, as an exotic species, it can affect native biota at different ecological
levels such as modifying population dynamics and community structure (MacGregor-Fors
et al. 2010). This species influences native bird species through dissemination of pathogens
that could affect humans and other species of birds (Vila et al. 2006). On the other hand,
behavioral studies have also shown that Columba livia has adapted its feeding timing to
human activities (Rose et al. 2006), and has become dependent on human resources
(McKinney 2002).
To characterize the urban gradient and heterogeneity in La Paz, we created six
urbanization categories based on a combination of the following characteristics: building
concentration, type of settlement (commercial areas, housing areas, crop areas, etc.), and the
presence of gardens and other green areas. As a result, we defined the following
urbanization categories: (1) Areas with natural vegetation, with no or few houses; (2)
Mainly crop areas, with native vegetation and few houses; (3) Areas that include green
areas for recreation, native and ornamental vegetation and few houses; (4) Residential areas
with many gardens; (5) Residential areas on hillsides (or not), with few green areas; and (6)
Mostly commercial areas with high percentages of impervious cover and low percentages
of vegetation cover. We assigned each observation station to one of these categories.
380 Urban Ecosyst (2010) 13:375–391

Data analysis

For each species, we obtained abundance (maximum number of individuals recorded at an

observation station in all three counts) and frequency of occurrence (number of observation
stations at which the species was recorded, divided by the total number of stations). Seven
species with wide home ranges were excluded from the analyses: five raptors (Variable
Hawk Buteo poecilochrous, American Kestrel Falco sparverius, Aplomado Falcon F.
femoralis, Peregrine Falcon F. peregrinus and Mountain Caracara Phalcoboenus mega-
lopterus), Yellow-billed Teal (Anas flavirostris) and the Andean Gull (Chroicocephalus
serranus) (Appendix). At each observation station we measured species richness, regarded
as the total number of species recorded in the three counts, and total abundance, regarded as
the sum of individual abundances of all the species present.
In order to compare bird species richness among urbanization categories, we performed
a rarefaction analysis for which we calculated the observed species richness for each
category (Sobs Mao Tau ±95% CI) and accumulated abundance using EstimateS (version
8.2) (Colwell 2009), as suggested by Gotelli and Colwell (2001). We used one-way
ANOVA to compare bird species richness and also bird abundances among urbanization
categories, followed by a Student-Newman-Keuls (SNK) post-hoc test, which is suitable for
difference in sample sizes.
To examine the effect that environmental and human activity measures have on bird
species richness and total abundance, we performed simple linear regressions. To assess the
combination of environmental variables that best explained bird species richness and bird
abundance, we used multiple regression analysis employing a forward selection model with
an F probability of 0.05 for entry and 0.01 for removal. We used the statistical program
SPSS® for Windows (version 15.0) to perform these analyses.
We used canonical correspondence analysis (CCA), a direct ordination technique that seeks
to explain variation in avian composition in terms of the measured environmental variables. To
perform this analysis, we used CANOCO® for Windows (version 4.5) (ter Braak and Šmilauer
1998). We used biplot scaling and interspecies distances in the ordination. The significance
of the CCA ordination was examined by performing 999 random permutation tests of Monte
Carlo. We used a manual forward selection procedure to identify the environmental variables
that best explained the variation in the bird species data. Variables were retained in
calculation of site scores when their addition significantly improved the fit of the CCA
model (P≤0.05). The relative contribution of selected variables to the explanatory power of
the CCA axes was determined by their intraset correlations (ter Braak and Šmilauer 1998).

Results

We registered and retained for the analysis 57 native bird species (Table 1, Appendix). Six
of the bird species had a frequency of occurrence of more than 50%: Rufous-collared
Sparrow (Zonotrichia capensis), Eared Dove (Zenaida auriculata), Chiguanco Thrush
(Turdus chiguanco), Black Siskin (Carduelis atrata), Peruvian Sierra-Finch (Phrygilus
punensis) and Sparkling Violet-ear (Colibri coruscans). These species, except Sparkling
Violet-ear were also the most abundant (Table 1). The high abundance of Greenish Yellow-
Finch (Sicalis olivascens) was mainly because it was observed in large flocks most of the
times. Six other species had a frequency of occurrence between 25 and 50%, and 45 species
had a frequency of occurrence of less than 25%. Names in English for all species are given
in Appendix.
Urban Ecosyst (2010) 13:375–391 381

Table 1 Bird species recorded in each urbanization category in La Paz, along with total abundance
(maximum number of individuals recorded at an observation station) and frequency of occurrence (number
of observation stations in which the species was recorded, divided by the total number of stations).
Nomenclature follows the South American Classification Committee of the American Ornithologists’ Union
(Remsen et al. 2009). Urbanization categories: (1) Areas with natural vegetation, with no or few houses; (2)
Mainly crop areas, with native vegetation and few houses; (3) Areas that include green areas for recreation,
native and ornamental vegetation and few houses; (4) Residential areas with many gardens; (5) Residential
areas on hillsides (or not), with few green areas; and (6) Mostly commercial areas with high percentages of
impervious cover and low percentages of vegetation cover

Urbanization category

Species Total abundance Frequency of occurrence 1 2 3 4 5 6

Patagioenas maculosa 24 14.4 x x x x x

Zenaida auriculata 224 68.3 x x x x x x
Metriopelia ceciliae 96 37.5 x x x x x x
Psilopsiagon aymara 19 4.8 x x
Aeronautes andecolus 5 3.8 x x
Colibri coruscans 89 53.8 x x x x x
Amazilia chionogaster 9 6.7 x x x
Patagona gigas 16 14.4 x x x x
Sappho sparganura 20 18.3 x x x x
Oreotrochilus estella 1 1 x
Lesbia nuna 1 1 x
Colaptes rupicola 18 14.4 x x x x x
Geositta punensis 2 1 x x
Geositta rufipennis 1 1 x
Cinclodes fuscus 14 8.6 x x
Leptasthenura fuliginiceps 3 2.8 x x
Leptasthenura aegithaloides 3 2.8 x x
Asthenes dorbignyi 57 36.5 x x x
Asthenes modesta 4 3.8 x x x
Ochetorhynchus ruficaudus 10 5.7 x x
Ochetorhynchus andaecola 4 3.8 x x
Anairetes parulus 9 8.6 x x x x
Ochthoeca leucophrys 8 4.8 x x
Ochthoeca oenanthoides 27 16.3 x x x
Muscisaxicola rufivertex 7 6.7 x x
Muscisaxicola cinereus 10 4.8 x x
Muscisaxicola alpinus 3 1 x
Muscisaxicola maculirostris 1 1 x
Knipolegus aterrimus 1 1 x
Phytotoma rutila 39 25.9 x x x x x
Pygochelidon cyanoleuca 15 5.8 x x x
Orochelidon murina 1 1 x
Troglodytes aedon 49 34.6 x x x x x
Turdus chiguanco 225 76.9 x x x x x x
Turdus fuscater 8 7.7 x x x x
Mimus dorsalis 19 7.7 x x
382 Urban Ecosyst (2010) 13:375–391

Table 1 (continued)

Urbanization category

Species Total abundance Frequency of occurrence 1 2 3 4 5 6

Thraupis bonariensis 14 5.8 x x x x

Thraupis sayaca 20 8.6 x x x
Conirostrum cinereum 5 2.8 x x x
Diglossa carbonaria 29 18.3 x x x x x
Diglossa brunneiventris 1 1 x
Zonotrichia capensis 501 91.3 x x x x x x
Phrygilus punensis 173 72.1 x x x x x x
Phrygilus fruticeti 26 19.2 x x
Phrygilus unicolor 3 1.9 x x
Phrygilus plebejus 18 10.6 x x
Poospiza hypochondria 21 13.5 x x x
Poospiza boliviana 2 1 x
Sicalis olivascens 218 27.9 x x x x x x
Sicalis flaveola 1 1 x
Catamenia analis 86 41.3 x x x x x x
Catamenia inornata 1 1 x
Saltator aurantiirostris 31 23.1 x x x x
Gnorimopsar chopi 3 1 x
Carduelis atrata 304 71.1 x x x x x x
Carduelis uropygialis 4 1.9 x x
Carduelis xanthogastra 40 13.5 x x x x

Bird species richness and abundance in relation to habitat and urban measures

Bird species richness varied significantly among urbanization categories (F5,103 =25.29, P<
0.001). Post-hoc tests (SNK) revealed that species richness in categories 6, 5 and 2 were
different among each other and from any other category; and that species richness in
categories 4, 3 and 1 did not differ from each other but were different from the rest of
categories (Fig. 2). Bird species richness decreased with increasing levels of urbanization,
with the highest value of species richness found in category 2, which represents crop areas
with native vegetation and few houses; and the lowest value was found in category 6,
commercial areas with high percentage of impervious surfaces and low percentage of
vegetation surfaces (Fig. 2).
Bird abundances also varied significantly among urbanization categories (F5,104 =6.72, P<
0.001; Table 2). They followed a similar pattern to that of bird species richness: bird
abundance was greatest in category 2 (33.2±16.3 individuals) and the lowest value in
category 6 (11±5.74 individuals) (Fig. 3). Post-hoc tests (SNK) showed that bird
abundances in category 2 were significantly higher than abundances in categories 5 and 6,
which did not differ from each other; abundances in categories 1, 3 and 4 were similar
among each other and with category 2; and finally, abundance in category 5 was similar to
abundances in categories 1, 3 and 4 (Fig. 3). Table 2 shows the differences among categories
in terms of number of stations, number of species, abundance and rarefied richness.
Urban Ecosyst (2010) 13:375–391 383

Fig. 2 Rarefied bird species richness in each urbanization category. Bars represent simulated 95%
confidence intervals (CI). Lower case letters next to each curve represent the groups created by ANOVA
post-hoc tests which compare bird species richness among urbanization categories. Curves that share the
same letter did not differ in species richness

Both bird species richness and abundance were significantly and positively related to
vegetation cover and native vegetation, and negatively related to built-up cover, abundance of
C. livia, pedestrian rate and car rate (Table 3). Multiple regression analysis selected two
variables that best explained bird species richness: vegetation cover and pedestrian rate (R2 =
0.52, F1,103 =53.901, P<0.001); and one variable that best explained bird abundance:
vegetation cover (R2 =0.423, F1,103 =22.178, P<0.001).

Bird composition in relation to habitat and urban measures (CCA)

The manual forward selection produced a model that consisted of three environmental
variables: elevation, built-up cover and native vegetation (Fig. 4). The relationship between
bird community composition and these environmental variables is displayed by a joint plot
of bird species scores (points) in relation to environmental variables (arrows) (Fig. 4). This
model explained 37.2% of the total variation in the species data. The first canonical axis

Table 2 Summary of bird species richness and abundance data in each urbanization category

Urbanization Number of Total number Mean richness Total Mean abundance Rarefied
category observation of species per observation abundance per observation number of
stations station station species

1 30 45 11.1 752 25.1 29.0

2 16 51 13.9 531 33.2 40.5
3 17 30 10.1 488 28.7 47.3
4 15 23 8.5 388 26 51.7
5 11 16 6.4 208 18.9 54.8
6 15 10 3.7 169 11 57.0
384 Urban Ecosyst (2010) 13:375–391

Fig. 3 Bird abundances in each urbanization category. Lower case letters represent the groups created by
ANOVA post-hoc tests which compare bird abundances among urbanization categories. Categories that share
the same letter did not differ in abundance

explained 21.7% of the total variation in avian composition; it represents an urbanization

gradient, characterized by built-up cover to the most urbanized right end and by native
vegetation to the less urbanized left end of the axis. The second canonical axis explained
11.3% of the total variation in the species data; it represents an elevational gradient with
higher and lower elevations to the upper and lower ends of the axis, respectively (Fig. 4).
The Monte Carlo tests showed that the ordination was significant, indicating that important
sources of variation in bird species data can be explained by the selected variables (F=1.45,
P=0.03).

Discussion

Urbanization has been shown to have serious negative effects on bird communities around
the world and the same is true for La Paz. Bird species richness and abundance decreased

Table 3 Results of linear regression analyses examining bird species richness and abundance in relation to
local habitat and urban development measures

Bird species richness Bird abundance

Measures Beta R2 P Beta R2 P

Elevation 0.049 0.002 0.621 0.044 0.002 0.66

Built-up cover −0.672 0.452 0.001 −0.383 0.147 <0.001
Vegetation cover 0.703 0.495 <0.001 0.423 0.179 <0.001
Native vegetation 0.372 0.139 <0.001 0.224 0.05 0.022
Pedestrian rate −0.535 0.286 <0.001 −0.373 0.139 <0.001
Car rate −0.342 0.117 <0.001 −0.196 0.038 0.046
Abundance of Columba livia −0.536 0.288 <0.001 −0.354 0.125 <0.001
Urban Ecosyst (2010) 13:375–391 385

Fig. 4 Ordination diagram defined by canonical correspondence analysis (CCA). The arrows represent the
environmental variables selected, and the diamonds represent the bird species. The direction of the arrows
indicates their correlation with an axis or a particular species. The length of the arrow represents the size of
the effect, the longer the arrow the stronger the relationship of that variable with the community (Lepš and
Šmilauer 2003). Total inertia (sum of the eigenvalues): 3.796. Elevation (ELEV) intraset correlation with
Axis 1: -0.0339 and with Axis 2: 0.7775. Built-up cover (BUILT) intraset correlation with Axis 1: 0.8398
and with Axis 2: -0.0271. Native vegetation (NATVEG) intraset correlation with Axis 1: -0.6079 and with
Axis 2: 0.2340. See Appendix for species codes

with increasing urbanization, a pattern seen in many studies in the northern hemisphere
(Beissinger and Osborne 1982; Clergeau et al. 1998; McKinney 2008) and within the
neotropics (Díaz and Armesto 2003; Leveau and Leveau 2004, 2005; Manhães and Loures-
Ribeiro 2005). Our results suggest that the variables we used as descriptors of local habitat
and urban development likely influenced patterns of bird richness and abundance. Species
richness was positively affected by vegetation cover, as reported in many urban systems
(Marzluff et al. 2001; McKinney 2002, 2008; Miller et al. 2003), including La Paz
(Garitano-Zavala and Gismondi 2003). Pedestrian rate has been shown in previous studies
to reduce richness of birds by modifying the likelihood of occupation and persistence
(Fernández-Juricic 2000; Schlesinger et al. 2008), although it can be positively related to
bird abundance (Ortega-Álvarez and MacGregor-Fors 2009). In our study, pedestrian rate
had a negative effect on species richness and abundance, but other environmental variables
such as vegetation cover, had a stronger effect. Another associated variable is car rate which
also affects bird richness because the noise generated by cars can interfere with bird
communication, leading to population and richness declines (Reijnen et al. 1997), a pattern
386 Urban Ecosyst (2010) 13:375–391

anecdotally suggested in the present study. Built-up cover also can influence bird
composition (Melles et al. 2003; Miller et al. 2003), likely because as urban development
increases the availability of resources is reduced. Abundance of C. livia in this study
influenced bird species richness, as reported previously (Garitano-Zavala and Gismondi
2003). Abundance of this species may not directly cause decline in overall species richness,
but it may represent a good predictor. Other variables such as noise or vegetation
composition should be taken into consideration to understand how and which aspects of
urbanization affect bird communities the most in La Paz, but this study provides an
important baseline for future studies.
The highest values of species richness and abundance were found in urbanization
category 2, where there is a mixture of crops, native vegetation and few houses. These
areas retain native shrub habitat, that may support some birds specialized to this
vegetation, as well as modified habitats (crop plants and exotic vegetation) that attract
other bird species. Crop areas in La Paz may constitute intermediate stages of
development, characterized by initial human impacts of suburban sprawl and only few
houses in a matrix of natural or agricultural habitat, that may allow for greater number
of species to persist compared to areas that show pre-development conditions
(McDonnell and Pickett 1990; Clergeau et al. 1998; McKinney 2002; Blair 2004; Crooks
et al. 2004).
Bird species respond to different levels of urbanization and this response likely
translates into the segregation of particular bird assemblages along an urbanization
gradient, as our study suggests. Our results are consistent with other studies in other
cities, in showing that urbanization causes the dominance of a small group of species
(Beissinger and Osborne 1982; Clergeau et al. 1998; Melles et al. 2003; Donnelly and
Marzluff 2006; Kark et al. 2007). Previous studies in La Paz also reported that urban
parks were dominated by a few species such as Rufous-collared Sparrow (Zonotrichia
capensis), Eared Dove (Zenaida auriculata), Chiguanco Thrush (Turdus chiguanco)
(Garitano-Zavala and Gismondi 2003). These species can survive and reproduce
successfully in urban environments because they use a diverse array of resources and
may be better able to tolerate human disturbance (Donnelly and Marzluff 2006; Kark et
al. 2007). These segregation patterns may also reflect dietary requirements, as these
species have broad requirements and are mainly omnivorous and granivorous (Chace and
Walsh 2004; Adams 2005; Kark et al. 2007; Schlesinger et al. 2008). In contrast,
increasing levels of development may be detrimental for species with narrower dietary
requirements, such as many insectivorous species (Bonier et al. 2007; Kark et al. 2007),
which may be restricted to or prefer less urbanized areas that retain higher propor-
tions of native vegetation. This seems to be the case for species such as Plain-
mantled Tit-Spinetail (Leptasthenura aegithaloides) or D’Orbigny’s Chat-Tyrant (Ochthoeca
oenanthoides) among many others. And finally some species are segregated to the middle
sections of this urbanization gradient such as Gray-bellied Flowerpiercer (Diglossa
carbonaria) or Golden-billed Saltator (Saltator aurantiirostris) which may prefer resources
such as flowers and fruits. We certainly did not specifically measured dietary
preferences, but such explanations may be inferred by the bird segregation patterns
found in our study.
Some of the species present in environments with high levels of urbanization, such as
Columba livia, are also very common in other South American cities, including in Chile
(Díaz and Armesto 2003), Argentina (Leveau and Leveau 2004, 2005; Faggi and
Perepelizin 2006) and Brazil (Manhães and Loures-Ribeiro 2005). The Rufous-collared
Sparrow (Zonotrichia capensis), for example, inhabits both natural and rural areas as well
Urban Ecosyst (2010) 13:375–391 387

as cities and other human settlements; in our study it was the most abundant native bird
species. The Eared Dove (Zenaida auriculata) is also a common species in urban and
suburban areas (Leveau and Leveau 2004). This process of supporting a small number of
widespread and successful species well adapted to human-dominated landscapes is termed
biotic homogenization and it represents a serious threat to biodiversity worldwide (Olden et
al. 2004; McKinney 2006; Rooney et al. 2007).
A very important pattern in La Paz is that composition of bird communities is not only
affected by urbanization but by the elevation gradient as well. Elevational variation in La
Paz has a fundamental influence in structuring bird communities; it determines an array of
different ecological conditions, vegetation structures and habitat types that provide greater
opportunities for resource subdivision (Terborgh 1977) because it is associated with factors
such as temperature or humidity. In our study, elevation gradient had a significant influence
on bird composition, with some species restricted to higher and some other species to lower
elevations. These changes reflect many factors that affect the distributional patterns of
individual species, such as changes in the resources present (Blake and Loiselle 2000).
Some species, such as the Sayaca Tanager (Thraupis sayaca) or the Gray-hooded Parakeet
(Psilopsiagon aymara) may be more common at lower elevations because of higher fruit
availability, a primary resource for these species. The distribution of the Sayaca Tanager is
also associated with the presence of gardens, which are more common at lower elevations
in La Paz and may provide different sources of fruit. The Brown-backed Mockingbird
(Mimus dorsalis) was also only observed at lower elevation environments, where thorn
scrub and cacti are common (Ribera 1991). At higher elevations, we recorded few exclusive
species such as the Andean Hillstar (Oreotrochilus estella), the Plumbeous Sierra-Finch
(Phrygilus unicolor) or the Bar-winged Cinclodes (Cinclodes fuscus), which rarely visit
habitats lower than 3,800 m (Ribera 1991). Finally, there are some ubiquitous species
present along the entire elevational gradient, such as the Rufous-collared Sparrow, the Bar-
Faced Ground-Dove (Metriopelia ceciliae) or the Rusty-vented Canastero (Asthenes
dorbignyi). It is important to highlight that elevation did not have an effect on bird species
richness, but this was probably because its influence is ameliorated by the stronger effect of
urbanization.
Our results are consistent with some global patterns of the impacts of urbanization on
birds; however, we report some patterns unique for La Paz. Bird species richness and
abundance decreased with increasing levels urbanization as we predicted. Bird communities
are also affected by urbanization as predicted, but additionally, there is an important effect
of the elevation gradient in structuring bird communities. Nevertheless, urbanization has a
stronger effect than elevation. The measures taken to describe local habitat and urban
development explained large amounts of variation in bird composition. Our knowledge of
the impacts of urbanization is still incipient and more research is needed to understand its
effects on biodiversity and ecological processes in the urban ecosystem of La Paz.
However, our research provides valuable information and constitutes a framework for
future studies.

Acknowledgements We thank John G. Blake, Pedro Blendinger, Bette Loiselle and Eliot Miller for
critically reviewing previous versions of the manuscript and for their valuable comments and contributions.
We also thank Charles Nilon, the Associate Editor of the journal and three anonymous reviewers whose
comments and suggestions were essential to improve the manuscript. We also thank Flavia Montaño-
Centellas for her contribution to earlier stages of this research. Mariana Villegas would like to thank Luis
Fernando Villegas for his help during the field work of the study. This research was funded by the Instituto
de Ecología of the Universidad Mayor de San Andrés in La Paz, Bolivia.
388 Urban Ecosyst (2010) 13:375–391

Appendix

Table 4 All the bird species recorded in the study, along with family, scientific name, name in English and
code

Family Scientific name Name in English Code

Anatidae Anas flavirostrisa Yellow-billed Teal ANFL

Accipitridae Buteo poecilochrousa Variable Hawk BUPO
Falconidae Falco sparveriusa American Kestrel FASP
Falco femoralisa Aplomado Falcon FAFE
Falco peregrinusa Peregrine Falcon FAPE
Laridae Chroicocephalus serranusa Andean Gull CHSE
Columbidae Patagioenas maculosa Spot-winged Pigeon PAMA
Zenaida auriculata Eared Dove ZEAU
Metriopelia ceciliae Bare-faced Ground-Dove MECE
Psittasidae Psilopsiagon aymara Gray-hooded Parakeet PSAY
Apodidae Aeronautes andecolus Andean Swift AEAN
Trochilidae Colibri coruscans Sparkling Violet-ear COCO
Amazilia chionogaster White-bellied Hummingbird AMCH
Patagona gigas Giant Hummingbird PAGI
Sappho sparganura Red-tailed Comet SASP
Oreotrochilus estella Andean Hillstar ORES
Lesbia nuna Green-tail Trainbearer LENU
Picidae Colaptes rupicola Andean Flicker CORU
Furnariidae Geositta punensis Puna Miner GEPU
Geositta rufipennis Rufous-banded Miner GERU
Cinclodes fuscus Bar-winged Cinclodes CIFU
Leptasthenura fuliginiceps Brown-capped Tit-Spinetail LEFU
Leptasthenura aegithaloides Plain-mantled Tit-Spinetail LEAE
Asthenes dorbignyi Rusty-vented Canastero ASDO
Asthenes modesta Cordilleran Canastero ASMO
Ochetorhynchus ruficaudus Straight-billed Earthcreeper OCRU
Ochetorhynchus andaecola Rock Earthcreeper OCAN
Tyrannidae Anairetes parulus Tufted Tit-tyrant ANPA
Ochthoeca leucophrys White-browed Chat-Tyrant OCLE
Ochthoeca oenanthoides D’Orbigny’s Chat-Tyrant OCOE
Muscisaxicola rufivertex Rufous-naped Ground-Tyrant MURU
Muscisaxicola cinereus Cinereous Ground-Tyrant MUCI
Muscisaxicola alpinus Taczanowski’s Ground-Tyrant MUAL
Muscisaxicola maculirostris Spot-billed Ground-Tyrant MUMA
Knipolegus aterrimus White-winged Black-Tyrant KNAT
Cotingidae Phytotoma rutila White-tipped Plantcutter PHRU
Hirundinidae Pygochelidon cyanoleuca Blue-and-white Swallow PYCY
Orochelidon murina Brown-bellied Swallow ORMU
Troglodytidae Troglodytes aedon House Wren TRAE
Turdidae Turdus chiguanco Chiguanco Thrush TUCH
Urban Ecosyst (2010) 13:375–391 389

Table 4 (continued)

Family Scientific name Name in English Code

Turdus fuscater Great Thrush TUFU

Mimidae Mimus dorsalis Brown-backed Mockingbird MIDO
Thraupidae Thraupis bonariensis Blue-and-yellow Tanager THBO
Thraupis sayaca Sayaca Tanager THSA
Conirostrum cinereum Cinereous Conebill COCI
Diglossa carbonaria Gray-bellied Flowerpiercer DICA
Diglossa brunneiventris Black-throated Flowerpiercer DIBR
Emberizidae Zonotrichia capensis Rufous-collared Sparrow ZOCA
Phrygilus punensis Peruvian Sierra-Finch PHPU
Phrygilus fruticeti Mourning Sierra-Finch PHFR
Phrygilus unicolor Plumbeous Sierra-Finch PHUN
Phrygilus plebejus Ash-breasted Sierra-Finch PHPL
Poospiza hypochondria Rufous-sided Warbling-Finch POHY
Poospiza boliviana Bolivian Warbling-Finch POBO
Sicalis olivascens Greenish Yellow-Finch SIOL
Sicalis flaveola Saffron Finch SIFL
Catamenia analis Band-tailed Seedeater CAAN
Catamenia inornata Plain-colored Seedeater CAIN
Incertae sedis Saltator aurantiirostris Golden-billed Saltator SAAU
Icteridae Gnorimopsar chopi Chopi Blackbird GNCH
Fringillidae Carduelis atrata Black Siskin CAAT
Carduelis uropygialis Yellow-rumped Siskin CAUR
Carduelis xanthogastra Yellow-bellied Siskin CAXA

Nomenclature follows the South American Classification Committee of the American Ornithologists’ Union
(Remsen et al. 2009)
a
Bird species were excluded from the analyses

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