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Ecological Indicators 85 (2018) 1068–1080

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Ecological Indicators
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Original Articles

Exploring temporal dynamics of urban ecosystem services in Latin America: T


The case of Bogota (Colombia) and Santiago (Chile)
⁎,1
Cynnamon Dobbsa, Ángela Hernández-Morenoa, , Sonia Reyes-Paeckea,b, Marcelo D. Mirandaa
a
Departamento de Ecosistemas y Medio Ambiente, Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, Av. Vicuña Mackenna 4860,
Santiago, Chile
b
Centro de Desarrollo Urbano Sustentable CEDEUS, Los Navegantes #1963, Providencia, Santiago, Chile

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

Keywords: Latin America is one of the most urbanized region in the world, where patterns of urbanization are disorganized
Urban-rural gradient and disjoint from urban planning, with unknown effects for ecosystem services (ES). We evaluated the ES in
Spatial patterns Bogota and Santiago for a 30-year period. Using remote sensing data, models and census data we quantified
Landscape metrics carbon regulation, climate mitigation and recreation potential. We assessed ES provision changes and their
Carbon
spatio-temporal patterns using landscape metrics. Urban vegetation patterns differ between the two cities be-
Urban ecology
cause of climate variability and greening policies. Bogota stored more carbon than Santiago given to climate
Recreation
effects, differences within city were the result of different policies and management. Climate mitigation showed
similar behavior for both cities, influenced by global climate, densification and urban sprawling. Recreation
potential increased in the inner-city and decrease at the outskirts, reflecting unplanned urban sprawling and
increase population. Areas of high ecosystem services connected for Bogota and fragmented for Santiago. Bogota
improved its environmental condition, as evaluated by ES provision, while Santiago worsens, even there was an
increased in vegetation cover. Vegetation cover was not a sufficient indicator for ecosystem services and the
distribution of it becomes highly relevant for informing mismatches between services and vegetation.

1. Introduction Convention on Biological Diversity, 2012). The ecosystem service fra-


mework is successful at linking humans and nature with applicability
More than 80% of the population in Latin America will be urban by for conservation, planning and policy. Ecosystem services can be used
year 2050 (UN-Habitat, 2011), increasing the pressure on natural re- as a communicating and policy tool for managing urban ecosystems,
sources. The explosive urban growth experienced during the twentieth and can contribute to climate mitigation and adaptation (Secretariat of
century had its peak in the 1980s, and started decreasing after reaching the Convention on Biological Diversity, 2012). Urban ecosystem ser-
2% nowadays (UN-Habitat, 2011). Unlike Asia and Africa, in Latin vices have been recognized as particularly relevant for improving
America and the Caribbean the urban transition process has been ba- human well-being, some examples from emerging economies can be
sically completed, therefore the changes occurring in their cities are no found in Porras et al. (2013) and Fisher et al. (2014).
longer driven by population growth, but by income growth and public Ecosystem service mapping is one of the key elements to enable
policies (Inostroza et al., 2013; UN-Habitat, 2011). Latin America is a decision-making and planning by recognizing their spatio-temporal
showcase for processes that are triggered by housing deficit, lack of dynamics (Burkhard and Maes, 2017; Crossman et al., 2012; Egoh et al.,
social infrastructure, and by the need to improve the life quality of 2008; Peña et al., 2015; Troy and Wilson, 2006). There are several
people that still lives in poverty. The social, ecological and environ- approaches for ecosystem service mapping, including social values
mental changes observed in the past three decades respond to a new (Bryan et al., 2010), distributions (Nelson et al., 2009), capacities,
stage of urban development in this continent (UN-Habitat, 2011), and economic values (Troy and Wilson, 2006), vulnerabilities (Schröter
could contribute to anticipate future urban processes for other world et al., 2005), supply and demand (Burkhard et al., 2011), among others.
regions. To improve urban planning is important to understand what are the
Given this, it is important that urbanization integrates into its long- effects of urbanization, either sprawling or densification, on the pro-
term planning the management of ecosystem services (Secretariat of the vision of ecosystem service at multiple scales (Haase et al., 2014).


Corresponding author at: Av. Vicuna Mackenna 4860, Macul, Santiago, Chile.
E-mail addresses: cdobbsbs@gmail.com (C. Dobbs), angelahernandez@uc.cl (Á. Hernández-Moreno).
1
Present address: Centro de Investigación en Ecosistemas de la Patagonia CIEP, Camino Baguales s/n., Coyhaique, Chile.

https://doi.org/10.1016/j.ecolind.2017.11.062
Received 19 June 2017; Received in revised form 22 November 2017; Accepted 28 November 2017
Available online 08 December 2017
1470-160X/ © 2017 Elsevier Ltd. All rights reserved.
C. Dobbs et al. Ecological Indicators 85 (2018) 1068–1080

Temporal studies of urban ecosystem services can aid in realizing those Table 1
patterns, disclosing information on the consequences of urban growth Population, socioeconomic data and built-up area Bogota and Santiago.
under local biophysical and socioeconomic conditions. This sort of re-
Bogota Santiago
search has been scarcely addressed (Kroll et al., 2012; Wu et al., 2011)
and it has been mainly based on land use/land cover changes. Population (inhabitants) 4,225,649 (1985) 3,902,329 (1982)
The availability of continuous data related with natural resources in 7,878,783 (2014) 6,348,770 (2014)
Built-up area (km2) 302 (1988) 383.6 (1986)
Latin America is scarce, therefore the use of remote sensing provides a
385 (2015) 617.2 (2014)
useful tool for quantifying ecosystem services dynamics in a spatially Population density (inh/km2) 20,464 10,286
explicit manner, and allows the comparison of how those services Population high income level (%) 4.4 11.3
changed over time. The quantification of the dynamics of ecosystem Population medium income level (%) 45.2 45.7
services can be assess through landscape pattern metrics which can Population low income level (%) 48.8 43
Administrative division 20 Localities 34 municipalities
inform on the variation along urban-rural and temporal gradients (Wu
et al., 2011). Frank et al. (2012) investigated the use of landscape Sources: Santiago population data INE Census 1982, 2002, projections 2002–2020;
metrics for appraising the potential of landscape to deliver ESS, Santiago Built up area 2000 Geo Santiago, PNUMA; Santiago Built up area 2014 own
showing that if landscape metrics are not considered, the potential of a data; Income level data Santiago Adimark S.A; Bogota: population data DANE, concilia-
landscape to provide ESS can be overestimated. Fürst et al. (2013) used tion census 1985–2005, Census 2005, projection 2006–2015. Bogota built-up area
a set of landscape metrics to assess the impact of land use patterns on Inostroza et al., 2013 (1988), Escobedo et al., 2016 (2015).

the potential of a region to provide ESS, and Frank et al. (2012) pre-
sented an approach on assessing landscape aesthetics with landscape
metrics. (Inostroza et al., 2013).
The purpose of this study is to understand the provision of urban These cities have experienced population growth since the mid-
ecosystem services and their spatio-temporal patterns occurring in the 1990’s until the late 2000’s resulting in sprawled urbanizations with
last 30 years for two Latin American cities: Bogota, Colombia and similar population (approximately 7 million for Bogota and Santiago;
Santiago, Chile. Both cities are representative of the succession of ur- Inostroza et al., 2013). These cities are good case study for illustrating
banization processes that have occurred in Latin America, especially in socio-ecological-spatial patterns occurring in Latin American cities,
the 20th century and after (Inostroza et al., 2013). This urbanization because both reflect the extreme income level disparities, socio-spatial
processes have left large areas of unplanned urbanization, with affluent segregation and the presence of densely populated neighborhoods along
areas characterized by low residential densities and poor areas char- the urban periphery (Kabisch et al., 2012).
acterized by social housing and self-constructed residences in high Bogota has an approximate area of 655 km2 and more than 7 million
densities, which has consequences for vegetation and ecosystem ser- inhabitants (www.dane.gov.co). The city is located at 2640 m.a.s.l, over
vices. the Western Andes Mountain Range plateau. Bogota has a temperate
We build a spatially explicit index that estimates the service of warm climate with tropical mountain vegetation type (Escobedo et al.,
global climate regulation, microclimate mitigation and recreation po- 2015), with mean annual temperatures ranging between 7 and 18 °C.
tential. We evaluate temporal changes in the provision of these eco- Rainfall is distributed throughout the year, with two main peaks be-
system services along an urban-rural gradient. Landscape metrics were tween April-May and September–November reaching 1400 mm per
used to assess spatio-temporal patterns on the ecosystem service index. year (De las Salas and García Olmos, 2000). Bogotá accounts for 15% of
Results from this research can improve our understanding of urbani- the population and contributes to more than 20% of national GDP.
zation on ecosystem service supply in understudied countries, detecting During the past three decades population has increased from 4.22 to
areas where environmental inequalities occur and relating them with 7.88 million inhabitants, while the urban area has increased at a lower
existing planning policies. rate from 302 km2 in 1988–385 km2 in 2015 (Inostroza et al., 2013;
Escobedo et al., 2015) reaching a population density of 20,464 inh./
2. Methods km2. Along the urban boundaries, the main land uses are agricultural
crops, forest plantations and grasslands; in the Eastern Mountain range
2.1. Study area there is a great diversity of native vegetation with remnant forests,
bushlands, and moorland in an altitudinal gradient. The Alcaldía Mayor
Bogota (Colombia) and Santiago (Chile) are capital cities and the (Bogota Major City Hall) oversees the environmental policy of the city,
economic, cultural and political centers of their respective countries. throughout its District Environmental Secretary (Secretaría Distrital de
They are intermediate size metropolises with population between 6 and Ambiente), that is responsible of the environmental policy and the city’s
10 million people (UN-Habitat, 2011). A summary of both cities char- Environmental Management Plan. In addition, the Botanical Garden
acteristics is detailed in Table 1. Jose Celestino Mutis, is the entity in charge of the design and im-
Bogota and Santiago are representative of the rapid urbanization plementation of the city’s urban forest.
processes, demographic transition and urban sprawl that characterize Santiago is in the central valley between the coastal and Andes
current development of Latin American metropolises (Hernández- mountain range, with a mean altitude of 650 m.a.s.l. The climate is
Gómez et al., 2013; De Mattos et al., 2014). Urban expansion during the temperate with dry summer (Csb) ranging between 8–30 °C. The annual
20th century left large areas of unplanned urbanization between 1950 rainfall reaches 350 mm and is concentrated in the winter months (May
and 1980’s, lacking of infrastructure and main utilities on their begin- to September). Santiago concentrates 36% of the country’s population,
nings (UN-Habitat, 2011). Since the 90’s both cities have a dual growth: contributes for about 42% of national GDP (INE, 2015). Its adminis-
low density residential in affluent areas that include large greenspaces, trative boundaries cover 2274 km2 of which 617 km2 correspond to
following North American suburbs patterns (Northern areas of Bogota built-up areas. Between 1985–2014 population has increased from 3.9
and Northwestern side of Santiago; UN-Habitat, 2011; Figs. 1 and 2). to 6.3 million inhabitants (INE, 2015) reaching a population density of
The second growth pattern included densely urbanized areas of social 10,287 in h./km2 in 2014 (Table 1). The urban area has increased at a
housing and self-constructions, where less affluent population estab- higher rate in the same period (from 383.6 to 617.2 km2), leading to a
lished. These peripheries lack of public greenspaces, but are common decrease in population density (Inostroza et al., 2013). The environ-
on vacant areas, wetlands, hills and agricultural land (Southern and mental policy of the city is overseen by several institutions including
northwestern periphery in Santiago and Bogota; Figs. 1 and 2). Both the Ministry of Environment, the National Forest Corporation, the re-
cities showed three urbanization forms: axial, infill and isolated gional government and all the municipalities within the city. The design

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Fig. 1. Study area and urban-rural gradient buffers for the city of
Bogota, Colombia.

and implementation of the city’s urban forest is overseen by each mu- 2.2. Image processing
nicipality apart from large public parks which are the duty of the
Ministry of Housing and Development through its greenspace depart- Landsat imagery (30 m pixel resolution) was used to detect vege-
ment. tated and non-vegetated areas, to then estimate the supply of key urban

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Fig. 2. Study area and urban-rural gradient buffers for the city of Santiago, Chile.

ecosystem services (Table 2). The images chosen were cloud free, and cloud free and allow us to compare the different dates more robustly
obtained from the Landsat archive (http://earthexplorer.usgs.gov/). All given their more stable atmospheric factors. No images were selected
images had radiometric and atmospheric corrections, an important pre- from years of strong ENSO effects. The years chosen reflects different
processing step for multi-temporal change detection (Chander et al., periods of urbanization: in the 80’s both cities are still compact and
2009). The images were chosen on the period of the year with the growing by occupying rural areas adjacent to urban edge, in the early
highest photosynthetic activity coinciding with the leaf on season of the 2000 low-density suburban developments appeared and urbanization
hottest time of the year. Dry season was used because the images were extends in all directions, and in present times urban growth occurs by

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Table 2
Characteristics of the satellite imagery for temporal analysis of Bogota and Santiago.

City Year Satellite Resolution Date

Bogota 1985 Landsat 5 TM 30 m multispectral pixel, 120 m thermal pixel (Band 6) 22nd March 1985
2001 Landsat 5 TM 30 m multispectral pixel, 120 m thermal pixel (Band 6) 29th January 2001
2014 Landsat 8 30 m multispectral pixel, 100 m thermal pixel (Band 10) 1st January 2014

Santiago 1986 Landsat 5 TM 30 m multispectral pixel, 120 m thermal pixel (Band 6) 12th November 1986
2000 Landsat 5 TM 30 m multispectral pixel, 120 m thermal pixel (Band 6) 18th November 2000
2014 Landsat 8 30 m multispectral pixel, 100 m thermal pixel (Band 10) 9th November 2014

infilling vacant lots remaining and new urban developments dispersed Celsius.
in peri-urban fringe. Recreation is probably one of the most recognizable services asso-
The red and infrared bands from the Landsat imagery were used to ciated with urban areas, because it provides for mental and physical
obtain NDVI (Appendix A in Supplementary material), commonly used enjoyment (Tzoulas et al., 2007). This study evaluates the recreation
for detecting biomass and photosynthetic capacity of vegetation and potential (supply) and not the demand given the temporal dimension of
widely used in urban areas (Dobbs et al., 2014; Faryadi et al., 2009). this research. We developed a recreation index that includes vegetated
The classification of the NDVI in vegetated and non-vegetated pixels areas over 1000 m2 because of their potential for multiple uses. Vege-
was based on the findings of (Stathopoulou et al., 2007), where va- tated areas were obtained from the NDVI/image classification process.
lues > 0.3 are consider vegetation and values < 0.3 are consider non- To represent this service, it was important to relate vegetation to po-
vegetated. The cutoff values were chosen to minimize the existence of tential users, linking vegetation to the amount of people by locality for
mixed pixels (Stathopoulou et al., 2007). Pre-processing and image Bogota and municipality for Santiago. We account for the aggregation
classification was done in ENVI 4.7 (Exelis Visual Information Solu- of the vegetation patches and the amount of those within administrative
tions, Boulder, CO). unit, by building a weighting factor as follows,

GAi NPi
2.3. Quantification of ecosystem services RPi = *
Pi ENNi
We selected the services of global climate regulation, microclimate where RP is recreation potential by administrative unit i, GA are the
mitigation and recreation potential using NDVI and commonly used and sum of all vegetated patches area over 1000 m2, NP is the number of
transferable methodologies (Dobbs et al., 2014). patches, ENN is the Euclidean nearest neighbor distance between pat-
Global climate regulation was selected because of its global impact ches (m) and P accounts for the population existing in i. In this calcu-
on climate (Strohbach and Haase, 2012) and linked to urban tree lation, we assigned a value of zero to the green areas located outside the
carbon storage that can aid in reducing the effect of CO2 release to the administrative units of the city, such as rural and mountainous areas,
atmosphere. It was calculated using a model that relates NDVI with given that those areas lack or population and inaccessibility.
carbon stored in urban trees of temperate US (Myeong et al., 2006). The For comparing ecosystem service supply between cities and dates it
model has been validated for cities, and has been used to quantify urban was important to re-scale the values for each service by the minimum
tree carbon for several cities around the world (Dobbs et al., 2014; and maximum value obtained, reaching a scale from 0 to 100 for each
Hutyra et al., 2011; Poudyal et al., 2010). The model assessed the service. All services then were summed in one map by date as follows:
functionality of the system and not its structure,
Ecosystem Service Index Datei = Global climate regulation + Microclimate
KgC ⎞ mitigation + Recreation potential
Carbon ⎛⎜ ⎟ = 107.2e
(NDVI * 0.0194)

⎝ pixel ⎠
No weight was assigned to the services because preferences on those
Microclimate mitigation, assess as the reduction in temperatures by were out of the scope of this manuscript. The range of the ES index goes
the presence of vegetation becomes relevant under urban heat island from zero when no services are provided in a pixel to 300 when the
and air pollution (Larondelle and Haase, 2013). We used the Land maximum supply value for all services is reached. The differences be-
Surface Temperature product (LST) to evaluate the differences in tem- tween dates were spatially assessed using the subtraction of the stan-
perature throughout the city and between periods of time (Jenerette dardized ecosystem service index to detect areas of increase and de-
et al., 2007). The calculation follows (Karnieli et al., 2010), crease of ecosystem services. All analyses were done in ArcMap 10
(LMAXλ − LMINλ ) (ESRI, Redlands, Ca).
Lλ = *(DN − QCALMIN ) + LMINλ
QCALMAX − QCALMIN
2.4. Urban-rural gradient analysis
where LMIN and LMAX are the spectral radiances, QCALMAX/MIN is
the quantized calibrated pixel value in DN (Landsat 5 and 7
We followed the classic urban-rural gradient analysis to identify and
QCALMIN = 0, QCALMAX = 255; Landsat 8 QCALMIN = 1,
evaluate the spatial variation of ecosystem service supply (Kroll et al.,
QCALMAX = 33518), DN is the pixel value and λ is the wavelength.
2012). This type of analysis is commonly used in urban studies for
Then the brightness temperature is calculated as follows,
understanding the changes in patterns and ecological processes due to
K2 urbanization (Andersson et al., 2007; Larondelle and Haase, 2013). To
T=
ln ( K1
Lλ )
+1 perform this analysis 5 km wide concentric rings from the city center
were created as follows 1) 5 K named city core, 2) 10 K named suburbs,
where K1 and K2 correspond to a coefficient determined by the effective 3) 15 K named peri-urban and 4) > 20 K named non-urban, this last
wavelength of the satellite sensor. For Landsat 5 TM K1 is 607.76 ring covers areas of prairies, agricultural land and natural forests. We
(Wm−2 sr−1 μm−1) and K2 is 1260.56 (Wm−2 sr−1 μm−1), for Landsat use these designated distances for comparison purposes to other urban
8 K1 is 774.89 (Wm−2 sr−1 μm−1) and K2 is 1321.08 studies of flora, fauna and land surface temperature which have also
(Wm−2 sr−1 μm−1). Finally, the values of temperature are converted to used the same distances (Clarkson et al., 2007; Hamer and McDonnell,

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2008; Kuang et al., 2014). For the city of Santiago, we used circular while the least gain happened in the peri-urban area. Santiago had an
rings, while for the city of Bogota semi-circles were used (Figs. 1 and 2). increase in urban tree carbon from 16.2 MgC/ha to 34.6 MgC/ha in the
The reason for using semi-circles in the case of Bogota is because the period between 1985 and 2000; secondly, carbon dropped to 6.6 MgC/
location of the city center is by the eastern mountain range where no ha from year 2000 to year 2014. For Santiago, the least loss occurred in
urbanization occurs, so there was no point on analyzing that area. For the city center, while the largest happened in the suburbs.
each ecosystem service the mean and standard deviation were calcu- Overall, Bogota showed a positive spatio-temporal gradient for the
lated for each ring. global climate regulation service, while Santiago showed the opposite
(Table 3).
2.5. Socio-economic gradient analysis
3.2. Microclimate mitigation
For both cities, we analyzed the ecosystem service index occurring
in three socio-economic categories: high, medium and low income ac- Both cities showed different trends in terms of microclimate miti-
cording to the definitions given by the census of each country gation. Bogota had a decrease in temperature of 2 °C for the whole city.
(Escobedo et al., 2006). For Bogota, the income classification was done In natural and rural areas (> 15 K from city center), the temporal
by ‘localidades’ and for Santiago by ‘comunas’. The classification for variability of temperature was less than the urban section.
Santiago was the same as the classification made by Escobedo et al. Temperatures in Santiago increased temporally for all the buffers,
(2006) for the city. For Bogota, official data classify population in six however, those increases were lesser in the city core and suburbs than
socioeconomic ‘estratos’ (1: low-low, 2: low, 3: medium-low, 4: in the peri-urban area and natural and rural areas (Table 3).
medium, 5: medium-high and 6: high income level) (Appendix B in
Supplementary material). In order to simplify the analysis, the socio- 3.3. Recreation potential
economic strata of Bogota was grouped in three classes named low
strata including strata 1 and 2, medium strata including strata 3 and 4, Bogota and Santiago showed a decreased in the recreation potential
and high strata integrating strata 5 and 6. for the whole city, with the largest decrease in the peri-urban and
natural areas. The city of Bogota, however, had a slight increase to-
2.6. Landscape patterns analysis wards the city core and suburbs. Santiago only showed an increased or
the city center, rising from 0.1 to 3.8 m2 per capita (Table 3).
To understand the spatial patterns of urban ecosystem service
supply we quantified commonly used landscape and class metrics for 3.4. Ecosystem service index
each concentric ring and for the whole city. The metrics included
number of patches, mean patch area, largest patch index, Euclidean Ecosystem service supply for Bogota changed by −6% from year
nearest neighbor and the Aggregation Index accounting for different 1985 to year 2001, to then increased 15.2% between year 2001 and
dimensions of the landscape, including measures of landscape compo- 2014 (from 131 to 151). The largest increased occurred in the city
sition, connectivity and configuration. In addition, these are some of the center and suburbs, changing 15% and 10% respectively. On each
most commonly used metrics in landscape ecology. A detailed de- period, the peri-urban area is the section that provides more services
scription for each metric can be found in (McGarigal et al., 2012). (159, 154 and 169 respectively). Bogota showed an increase in the
Calculations were done in FRAGSTATS V4. index for all the urban-rural gradient sections. The largest increment
To evaluate the spatial pattern of the ecosystem service index we occurred at the city center and the smallest increase happened in the
divided the index in three levels of provision: low (0–100), moderate peri-urban area (Fig. 3).
(100–200) and high (200–300). The purpose of this classification was to Ecosystem service supply for Santiago showed a different trend to
evaluate changes in fragmentation (Fahrig, 2003), distribution and Bogota. The overall value for ecosystem service supply decreased by
composition of the service supply along the period of analysis. 17% from year 1986–2014 (from 175 to 149), where the lowest supply
occurred at the city center, while the largest supply was in the suburbs
3. Results and peri-urban sections. The only increase in the index happened in the
suburbs, while the largest decrease occurred in the peri-urban area
The spatio-temporal change of vegetation cover is presented in (Fig. 4).
Table 3. Bogota excluding the rural and natural areas in the gradient The spatial distribution of ecosystem service supply for both cities
(> 15 K), had a 28.6% vegetation cover in year 1985, and then de- appears in Figs. 3 and 4, disclosing their temporal dynamics. For Bo-
creased to 11.3% in 2001, to then have an increment to 27.4% in 2014. gota, the increase in ecosystem service supply can be interpreted as
In contrast, rural and natural areas (> 15 K) showed a reduction in having a poor supply in year 1985 close to the city center to an increase
vegetation cover of almost 10% (Table 3). The largest shift occurred in of the supply across all the city for year 2014 (Fig. 3). There was a slight
rural areas, while an increase in vegetation cover in year 2014 occurred decrease in the index towards the east of the city and the south, close to
in the core area and the suburbs. Santiago, excluding rural and natural the eastern mountain range. For Santiago, there was a reduction and
areas in the gradient, had a vegetation cover of 3.2% on year 1986, more heterogeneous distribution of the ecosystem service supply from
increasing to 4.2% in year 2000, and then decreasing to 3.6% in 2014. year 1986 to year 2014 (Fig. 4). The largest change occurred in the peri-
The major increase in vegetation cover occurred in the natural area for urban and natural area (Fig. 4).
the whole analyzed period. The socio-economic analysis for the city of Bogota did not show
major differences in the value of the index for the period of analysis.
3.1. Global climate regulation Changes in the value of the index between 1985 and 2014 showed an
increase for most localities and the magnitude of changes was similar
The total carbon stored by vegetation for the city of Bogota in 2014 for all the socio-economic classes (Table 4). Lower strata showed an
corresponded to 23210 KT (699 MgCO2/ha), while the city of Santiago improvement in the localities adjacent to rural and natural areas, al-
stored, in 2014, 6929 KT (110 MgCO2/ha). Urban tree carbon storage though two of the poorest localities (Localities of Bosa and Usme, Ap-
in Bogota showed two trends. Firstly, there was a decrease in carbon pendix B in Supplementary material) showed a decrease in the index
storage from 21.2 MgC/ha in 1985–20.5 MgC/ha in 2001 to then in- value.
creased to 25.2 MgC/ha by year 2014, overriding the initial value by Contrarily for Santiago, there are differences in the index according
16%. The largest gain for Bogota occurred in the core and suburbs, to the socio-economic strata (Table 4). High income communes have

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Table 3
Vegetation cover and ecosystem services for the whole city and the urban-rural gradient of Bogotá and Santiago corresponding to three dates in a 30-year period. Standard deviation is
shown in parenthesis.

Bogotá Santiago

1985 2001 2014 1986 2000 2014

Vegetation cover (%)


Whole city 75.6% 54.9% 67.2% 45.1% 58% 57.8%
5K 15.8% 5.2% 16.5% 0.2% 0.5% 0.4%
10 K 22.3% 7% 23.4% 2.2% 3.5% 2.4%
15 K 47.9% 21.8% 42.4% 7.2% 8.6% 8%
> 20 K 94% 73.9% 83.5% 35.4% 44.3% 46.6%

Global climate regulation (MgC/ha)


Whole city 21.2( ± 7) 20.6( ± 8) 25.2( ± 11) 16.2( ± 4) 24( ± 4) 6.8( ± 3.4)
5K 19.7( ± 3) 22.5( ± 4) 28( ± 7) 6.9( ± 0.8) 11.5( ± 1.8) 6.9( ± 2.8)
10 K 20.1( ± 4) 22.1( ± 4) 27.2( ± 6) 23.2( ± 1.1) 16.5( ± 2.3) 6.8( ± 2.8)
15 K 21.5( ± 5) 23.4( ± 4) 28( ± 7) 8.4( ± 4) 27.6( ± 3.3) 6.7( ± 3.7)
> 20 K 24.4( ± 5) 26.5( ± 5) 32.2( ± 6) 19.6( ± 5) 40.3( ± 4) 6.6( ± 3.2)

Micro-climate mitigation (Celsius)


Whole city 23( ± 5) 20( ± 4) 21( ± 5) 30( ± 2) 31( ± 5) 34( ± 4)
5K 24( ± 3) 21( ± 3) 26( ± 4) 32( ± 2) 33( ± 2) 35( ± 1)
10 K 25( ± 3) 22( ± 2) 26( ± 4) 30( ± 2) 32( ± 2) 35( ± 2)
15 K 26( ± 3) 22( ± 3) 24( ± 3) 28( ± 3) 30( ± 3) 34( ± 4)
> 20 K 22( ± 5) 20( ± 4) 21( ± 5) 28( ± 4) 29( ± 9) 34( ± 5)

Recreation Potential (m2/per capita)


Whole city 113( ± 161) 53.8( ± 73) 66.9( ± 82) 16.9 ( ± 480) 2.8( ± 1.2) 3.2( ± 3)
5K 4.8( ± 8.5) 2.8( ± 6.2) 6.7( ± 9.5) 0.7 ( ± 1.2) 0.1( ± 0.07) 3.8( ± 2)
10 K 6.2( ± 8.2) 0.8( ± 1.1) 7.6( ± 7.4) 9 ( ± 23) 0.5( ± 1.1) 1.3( ± 2.7)
15 K 131( ± 66) 54( ± 52) 77.7( ± 66) 12.9 ( ± 8) 3.9( ± 1.3) 3( ± 4)
> 20 K 309( ± 203) 158( ± 50) 175( ± 60.4) 72.4 ( ± 9) 6.5( ± 3) 4.5( ± 4)

the most improvement in the index value between years 1986 and 3.5. Ecosystem service index landscape metrics
2014, with only one commune showing a decrease in the index. The
main decreases in the index occurred in the low-income communes, Table 5 illustrates the changes in landscape metrics in Bogota and
where less than half of the communes showed an improvement in the Santiago for the analyzed period, according to three ecosystem services
index. supply classes: low, moderate and high.
In Bogota, the percentage of the landscape covered by low and high

Fig. 3. Ecosystem service supply for the city of Bogotá (years 1985–2001–2014). The index is constructed by three ecosystem services: global climate regulation (regulation function),
micro-climate mitigation (regulation function) and recreation potential (cultural function). Urban-rural gradient buffers are added to facilitate analysis.

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Fig. 4. Ecosystem service supply for the city of Santiago (years 1986–2000–2014). The index is constructed by three ecosystem services: global climate regulation (regulation function),
micro-climate mitigation (regulation function) and recreation potential (cultural function). Urban-rural gradient buffers are added to facilitate analysis.

class of supply varied, while for the moderate class the supply remained 2003 the city was governed by 10 different mayors from different po-
similar. For the whole period of analysis, the low provision decreased in litical views with government cycles lasting 1 or 2 years. In 2002, this
6%, while the change for the high provision was positive, increasing by changed and 4 years’ government periods were established leading to a
7%. The patch number and the mean patch area showed similar trend, continuity in policies. Given this, Bogota showed a slight recovery in
the low provision class had a change in −45% and −17% respectively. vegetation cover because of strong public policies stated since the
Contrary the high provision class change in +53% and 26% for the 2000’s as shown in Table 3. The largest changes in vegetation for both
number of patches and their mean area for the whole period of analysis. cities occurred in the non-urban area and the suburbs. As Schneider and
The high provision largest patch increased in the same proportion Woodcock (2008) suggested, South American cities present a behavior
(∼4.5%) as the low provision largest patch decreased. The nearest similar to United States cities, where most of the changes in the land-
neighbor metric only showed a relevant change for the low provision scape occur at the fringe and near cities core.
class, through an increase in the distance between patches of 17%,
while the other two classes (moderate and high) did not showed 4.1. Carbon regulation vs. climate, policies and management
changes over 5% (Table 5).
The percentage of landscape metric for Santiago changed largely for When comparing carbon values between Bogota and Santiago it is
the low and high provision classes, +41% and −34% respectively. possible to distinguish a climate effect, with Bogota storing around 3
There was a considerable decreased in the number of patches for the times more carbon than Santiago (≈23000KT vs 6900KT respectively
high provision class and an increased for the low provision class for the for year 2014). The spatial variation in both cities, however can be a
whole period of analysis. The mean patch in the low provision class combine effect of green policies and management with climate, dis-
duplicated its area between 1986 and 2014, while for the high provi- closed by the variability on storage within city, as shown by other
sion class there was a reduction in 50% of the size. The largest patch global studies (Dobbs et al., 2014).
index increased its size by 30% in the low provision lass, while the Results showed that Bogota had values of urban tree carbon for
other two classes decreased their sizes around the 20%. The main 2014 (between 32–25 MgC/ha) similar to urban forests of subtropical
changes in the nearest neighbor distance occurred for the moderate and cities such as Gainesville, FL (Escobedo et al., 2010), Xiamen, China
high provision classes. The moderate class the distance to the nearest (Ren et al., 2011) and cities in Korea (Jo, 2002). Clerici et al. (2016)
patch of the same class doubled, while for the high class it had an in- reported values of 6–50 MgC/ha in Bogotás peri-urban secondary for-
crement of 500 m (Table 5). ests in the eastern and northern mountainous areas. Santiago values
(6.6 MgC/ha) for 2014 were more similar to other Mediterranean and
4. Discussion semi-arid urban forests, such as Barcelona (approx. 14 MgC/ha;
Chaparro and Terradas, 2009) and Arizona (4.4 MgC/ha; Nowak and
Latin American research on urban ES can inform on the con- Crane, 2002), while Escobedo et al. (2016) reported values for Santiago
sequences of unplanned urbanization and the effect of peri-urban in- of 6–21 MgC/ha.
formal settlements by spatially and temporally determining the pre- There was no clear link between vegetation cover and the urban tree
sence and quantity of ES. carbon stored for the two studied cities, our results do not show that
Few studies have assessed these urban ecosystem services spatio- increases in vegetation resulted in increases in carbon stored (Table 3).
temporal patterns in Latin America and the results showed that, even This could be explained by the vegetation condition, given that the
Bogota and Santiago have similar historical origins; their urban vege- urban tree carbon model relies on NDVI, therefore the photosynthetic
tation dynamics are different, showing a possible effect of the climate capacity of woody vegetation. The decrease in carbon for Bogota was
and governance. associated with less vegetation cover, contrary to what happens for
The large reductions in vegetation cover in the most urbanized areas Santiago. Even Santiago has an increased in vegetation cover there was
of Bogota (core and suburbs) between years 1985 and 2001 could be a decreased in carbon values for the last period of analysis, which could
explained by the lack of continuity in the city governance and therefore be explain by temperature and precipitation effects. Since 2007, the
in the application of environmental policies. Between years 1985 and Mediterranean region of Chile has been subjected to a long period of

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Table 4 and appearance of informal settlements. The temporal analysis showed


Distribution of ecosystem service index by income for each year of analysis. that Bogota increased its temperature difference between the urban
core and the natural area from 2 °C in 1985–5 °C in 2014, but kept it
City Income Locality/Comunne T1 T2 T3 Change T1-T3
under the lower bound of what has been shown for large cities (2–7 °C;
Bogota Low Bosa 159 169 153 −6 Seto and Shepherd, 2009). After 1985, there was a large increase in
Ciudad Bolivar 173 191 197 24 population derived from rural migration caused by armed internal
Rafael Uribe Uribe 107 117 131 24
conflicts affecting mainly peri-urban areas. This led to uncontrolled and
San Cristobal 150 172 168 18
Santa Fé 157 138 188 30 illicit urbanization around the peri-urban and rural and natural sections
Tunjuelito 106 115 142 37 affecting land use and therefore temperature (Escobedo et al., 2015).
Usme 175 180 174 0 Further from this, unplanned urban sprawling has occurred in the
Medium Antonio Nariño 94 106 118 24 natural areas, increasing impermeable surfaces and intensifying the
Barrios Unidos 130 92 130 0
urban heat island effect. On top of this there is a global effect of the
Candelaria 109 113 114 5
Engativa 153 160 169 16 ENSO phenomenon on the urban and natural temperatures (Golden,
Fontibón 175 166 174 0 2004), as can be seen by higher temperatures in rural and natural areas
Kennedy 141 151 158 17 between the years of analysis.
Los Martires 100 102 114 13
Similarly, Santiago was influenced by the same factors: global cli-
Puente Aranda 123 100 147 23
Suba 197 147 214 17 mate, densification and urban sprawling. The city showed a decreased
Teusaquillo 139 97 160 21 in temperature differences between the urban and rural and natural
High Chapinero 179 149 182 3 areas from 4 °C in 1986–1 °C in 2014, therefore urban sprawling and
Usaquen 192 146 200 7 densification occurring in the peri-urban and rural and natural areas
Santiago Low Quilicura 137 168 203 66 (Inostroza et al., 2013). Both cities showed similar patterns on the cli-
Pudahuel 234 184 194 −40 mate regulation service, however temperature values were much higher
Huechuraba 149 144 179 30
for Santiago. For this city, there was a cofound effect of Mediterranean
Conchali 135 149 105 −30
Recoleta 135 133 131 −4 climate together with uncontrolled urban sprawling (Inostroza et al.,
Renca 135 157 139 4 2013).
Cerro Navia 135 134 106 −29
Quinta Normal 135 133 117 −18
Lo Prado 133 111 119 −14
Estacion Central 134 129 133 −1
4.3. Recreation potential vs. population and policies
Pedro Aguirre Cerda 132 118 122 −10
Cerrillos 133 143 168 35 Urban ecology has shown that recreation is not only related to the
Lo Espejo 133 97 111 −22 quantity of green spaces but also to its distribution and accessibility and
La Cisterna 132 112 126 −6
the method used here accounts for all. Given that if green spaces are
La Granja 132 99 123 −9
San Ramon 131 97 113 −18 more separated in distance and are only in few patches then less people
El Bosque 133 115 146 13 might have access to them (Fuller and Irvine, 2010).
La Pintana 142 136 150 8 The city center for both cities showed an improvement in the re-
Puente Alto 141 154 154 13 creation service, with Bogota showing better values than Santiago. This
Medium Maipu 140 180 168 28
San Bernardo 137 178 198 61
could be explained by renovations occurring at the city center, where
Independencia 136 126 119 −17 public spaces regain terrain (Borsdorf and Coy, 2009). However, both
Santiago 134 127 119 −15 cities have values under the recommendation of other researchers
San Miguel 133 117 133 0 (Sukopp et al., 1995; Wang, 2009). Despite these values been under the
San Joaquin 134 111 103 −31
recommended, some studies showed that in Bogota people recognize
Macul 134 131 168 34
Peñalolen 135 146 153 18 and value the benefits of the green spaces existing adjacent to their
La Florida 130 141 145 15 houses (Parra et al., 2010; Scopelliti et al., 2016). In the suburbs of
High Lo Barnechea 230 178 197 −33 Santiago there was a decrease in the service given an increment of the
Vitacura 136 173 172 36 built-up area without increasing green spaces (Banzhaf et al., 2013).
Las Condes 132 167 151 19
La Reina 135 159 160 25
The peri-urban area had the highest value for this service coinciding
Ñuñoa 136 136 158 22 with high income areas, commonly known pattern from green spaces in
Providencia 134 142 143 9 Latin American cities.
In peri-urban and rural and natural areas both cities decrease the
value for this service, because of population growth and land use
change, leading to urban sprawling, more profoundly in Santiago than
drought because of La Niña (Roco et al., 2015), affecting the photo- in Bogota (Banzhaf et al., 2013; Inostroza et al., 2013). For both cities,
synthetic capacity of plants, factor affecting NDVI values (Karnieli the population doubled between years 1986–2014, without being ac-
et al., 2010). companied by adequate green space planning that would have ensured
the maintenance of this service in areas of new development. This si-
4.2. Climate regulation vs. urbanization tuation is less abrupt for Bogota, where strong initiatives of land re-
storation and reforestation have avoided a large loss of green spaces in
The presence of vegetation in urban areas influences the service of new development areas (Boletin REDCRE, 2015). This could be
climate regulation. In addition, there are other factors such as the showing that when having good policies in place, in addition to the
global climate phenomenon (ENSO), densification, increase impervious proper institutional capabilities, the supply of this service could be less
surfaces and urban sprawling can also affect temperatures (Golden, affected, even with increasing population. However, large values in the
2004; Zhou et al., 2011). peri-urban and rural and natural area in Bogota could be influenced by
Bogota showed the typical trend occurring in urban climate, where the existence of agricultural land and forests located at the fringes
higher temperatures occur in more urbanized areas (Coutts et al., (Fig. 1), confirmed by the large standard deviations for this service
2010). There was an increase in temperature between 1985 and 2014, (Table 3).
which is a combination of densification, increase impervious surfaces

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Table 5
Landscape metrics occurring in the urban-rural gradient and the whole city for Bogota (years 1985–2001–2014) and Santiago (years 1986–2000–2014).

Number of patches Mean patch area Largest patch index Nearest Neighbor Percentage of the landscape

Bogota Low provision 1985 6009 2.7 4.9 91.5 13.7


Moderate provision 1985 2301 43.6 80 77.5 82.3
High provision 1985 1764 2.6 0.7 111.6 3.9

Low provision 2001 5456 5.5 6 82.2 24.7


Moderate provision 2001 3996 22.4 69.5 79.7 73.4
High provision 2001 1084 2.0 0.8 125.6 1.7

Low provision 2014 4155 2.4 0.7 110.6 8.1


Moderate provision 2014 2058 47.6 78.8 80.5 80.2
High provision 2014 3793 3.7 5.6 106 11.3

Santiago Low provision 1986 348 3.3 0.3 439.6 0.5


Moderate provision 1986 681 216.6 63.9 155.9 64.3
High provision 1986 1618 50 21.7 85.6 35.2

Low provision 2001 3979 38.8 64.2 77.1 66.2


Moderate provision 2001 13254 5.7 11.5 98.2 32.4
High provision 2001 2117 0.7 0.03 110.2 0.64

Low provision 2014 1339 70.2 29.9 345.9 41.7


Moderate provision 2014 853 150 49.1 336.6 56.7
High provision 2014 149 25.7 0.3 521.6 1.7

4.4. Ecosystem service index spatio-temporal pattern important factors that can inform on mismatches between both. For
example, in the city center of Bogota there was an increased in vege-
The socio-economic analysis of the ecosystem service index for tation cover of less than 5% and an increased in ecosystem service index
Bogota did not show any effect in their magnitude and distribution. of nearly 20%, while for Santiago there was an increased in vegetation
This result could be influence by the scale of analysis done at the lo- cover by 50% in the city center, and a decreased of the ecosystem
cality level, different from the socioeconomic strata which covers only a service index of nearly 10% (Fig. 5).
block. This scale effect does not allow for the index of ecosystem service Bogota and Santiago showed different spatio-temporal patterns of
to clearly show the effects of socioeconomics on the provision of eco- fragmentation of ecosystem services, this could be linked to the model
system services in Bogota which is highly fragmented. This socio- describe by Borsdorf and Coy (2009) for the fragmentation of Latin
economic fragmentation can be observed in Appendix B in American cities, where the fragmentation is result of social inequalities.
Supplementary material where one locality could have 2 opposed strata Bogota decreased its fragmentation for the high service provision class,
(Localidad Antonio Narino and Usme, Appendix B in Supplementary while Santiago showed an increased for the same class. This shows that
material) or even 6 different socioeconomic strata (Localidad de ecosystem services can respond differently to fragmentation (Mitchell
Chapinero, Suba and Usaquen). According to our scale of analysis, et al., 2015). The temporal pattern of ecosystem service supply for
improvements that occurred in the lower economic strata in the Bogota and Santiago showed that fragmentation is not always negative,
mountainous region could be due to changes in climate more than a and that the fragmentation of vegetation does not always result in a
socio-economic effect. Increases of the index in the urban core and fragmentation of the service.
suburbs could be due to afforestation programs on public green spaces. Spatio-temporal patterns for Bogota showed that areas with low
Contrarily, Santiago showed a socioeconomic effect, where social service provision class fragmented, while the areas of high provision
inequalities matched environmental inequalities represented by lower class decreased their fragmentation (Table 5). Bogota had an im-
provision of ecosystem services. Ecosystem service index for Santiago provement of its environmental condition, due to the increased of the
became worst in the communes from lower socio-economic classes, high provision patches and decreased of their fragmentation. This could
resulting from low greening budgets, high density urbanization and a reflect the good environmental public policies that have been applied in
dry landscape. More affluent areas showed an increase of ecosystem the last years (see previous section). Santiago showed the opposite re-
service index, where the only decrease occurred in a peri-urban com- sults, where there was a fragmentation of the high provision class and a
mune subjected to urbanization in the last 15 years. The decrease of the decreased in the fragmentation of the low provision class (Table 5).
index in centric communes could be the result of urban renewal policies Santiago had a detriment of its environmental condition, due to the
implemented in the early 90s, which promoted high-rise apartments to fragmentation of the high provision class. However, this is not only the
avoid the loss of population in the city center (Banzhaf et al., 2013) and reflection of weak environmental public policies but also a consequence
poor public environmental policies (Romero et al., 2012). The different of global climate change (ENSO), where by year 2014, the city had been
patterns of fragmentation occurring in the suburbs, peri-urban and non- subjected to long drought period (Roco et al., 2015). For both cities,
urban areas of Bogota and Santiago could be explained by their dif- there was a positive outcome of transformation, i.e. the spatial dis-
fering informal settlement patterns. Bogota has a larger presence of tribution of ecosystem services become more equal, where high provi-
informal settlements than Santiago (13% and 8% respectively). The sion class patches can be found in all the urban-rural gradient and not
spatial distribution of those settlements also differs among cities, while only restricted to the peri-urban and rural and natural areas (Figs. 3 and
Bogota’s informal settlements appear compact, Santiago’s informal 4).
settlements showed a highly fragmented and diffuse pattern (Inostroza, To understand the differences in the spatio-temporal dynamics of
2017) affecting differently the spatial distribution of ES. ecosystem services, further from climate differences, for both cities it is
In Fig. 5 we can distinguished that the amount vegetation cover necessary to recognize the different institutional structure that both
alone is not a sufficient indicator for ecosystem service provision and cities have. As a capital city Bogota is governed by the “Alcaldía
that the distribution and condition of the vegetation becomes also Mayor”, institution that integrates the administration and governance

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Fig. 5. Temporal changes relative to the latest year on the ecosystem services index and vegetation cover along an urban-rural gradient for the cities of Bogota and Santiago. The
ecosystem service index is composed by values for global climate regulation, micro-climate mitigation and recreation potential. Positive values indicate an increased in ecosystem service
index or vegetation cover in the period of analysis.

of 20 localities. On the contrary, Santiago does not have a unique spatio-temporal variation of ecosystem services and urbanization in
government that rules all the municipalities of the city; comprising 34 Latin America, shedding some light on the consequences of rapid urban
administrative units with their own mayor, independency in adminis- growth in highly dynamic and unplanned urban systems. This spatial
tration and management (Escobedo et al., 2006). The institutional approach could inform better planning for the reduction of environ-
structure of Bogota delivers same policies and visions for the develop- mental inequalities, one of the main issues in Latin American countries.
ment of the whole city, while for Santiago this is fragmented and sev- This study allows understanding the changes in temporal patterns of
eral policies and the management is differently decided for the 34 ecosystem services in urban landscapes, using the landscape ecology
municipalities, increasing heterogeneity of development. framework. The recognition of patterns of ecosystem services is re-
levant because they reflect the social conditions and the environmental
4.5. Limitations and future research public policies; reflect the social hierarchies and social activities.
Both Latin American cities showed different urban growth dy-
All the methods used in this study have the purpose of assessing the namics, but both showed the influence of urbanization and climate. The
general trend in the provision of ecosystem services for both cities in an consequences of urban migration and lack of planning caused different
understudied region, that said, we noted that there are limitations in patterns in the ecosystem service index for both cities resulting from
our analysis given the available data and model utilized. We note, that different governance systems, Bogota a more integrative system and
the scale of analysis is not going to inform on which type of vegetation Santiago a more independent local government system.
is providing the service or on who is receiving the service, the resolu- Results from this study discloses that future research should aim at
tion of the Landsat (30 × 30 m pixel) does not allow distinguishing integrating more social variables in the analysis of ES, such as the
between a tree or grass, or the type of land use that is around a patch of governance system, real estate market, among others. This will enable a
vegetation. More detail studies on ES should include a less sparse better understanding of ES positive interactions between the social and
analysis and better spatial resolution. ecological dimensions of urban development, by identifying causal re-
The quantification of ES can also be improved by using locally de- lationships and not just patterns.
veloped carbon models and finer resolution data that are able to dis-
tinguish the type of vegetation storing the carbon (Clerici et al., 2016). Appendix A. Supplementary data
In addition, it needs to be recognized that the model is based on tem-
perate urban forests and only accounts for tree aboveground carbon, Supplementary data associated with this article can be found, in the
disregarding the other forms of carbon dynamics (i.e. belowground online version, at https://doi.org/10.1016/j.ecolind.2017.11.062.
carbon, soil carbon, among others). The assessment of recreation po-
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