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Land Use Policy 42 (2015) 609618

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Land Use Policy


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

National ecosystems services priorities for planning carbon and water


resource management in Colombia
N. Rodrguez a, , D. Armenteras a , J. Retana b
a
Laboratorio de Ecologa del Paisaje y Modelacin de Ecosistemas, Departamento de Biologa, Facultad de Ciencias, Universidad Nacional de Colombia,
Carrera 30 No. 45-03, Bogot, Colombia
b
Centre de Recerca Ecologica i Aplicaciones Forestals i Unitat dEcologa, Universitat Autnoma de Barcelona, Campus de Bellaterra, 08193 Cerdanyola del
Valls, Bellaterra, Catalonia, Spain

a r t i c l e i n f o a b s t r a c t

Article history: The modelling and mapping of ecosystem services (ES) are important components of any programme
Received 18 July 2013 of land management planning, as they help evaluate the potential benets that ecosystems provide to
Received in revised form 29 May 2014 society. The objective of this paper is to evaluate ES for setting priorities and planning carbon and water
Accepted 17 September 2014
resource management in Colombia. By using information related to provision and regulation services
for water, carbon storage and protection services against extreme events such as landslides, we have
Keywords:
evaluated the spatial distribution of ES and identied geographical hotspots. The results are presented
Carbon storage
for two levels of analyses: (1) natural regions and (2) watersheds. We found differences in the distribution
Water provision
Ecosystem services mapping
and range of values for ES and observed that each region and watershed tends to maximise one or two
Watershed services, with the exception of the Caribbean region, which presents low values for most services. The
Planning services of water resources provision, regulation of water ow and carbon storage in the above-ground
biomass presented high correlations among them, with the Pacic and Amazonian regions presenting the
highest average values for these ES. The Andean region was important for the prevention of landslides
and the amount of carbon in the soil. At the watershed level, the Amazon watershed and those associated
with transition areas (piedmont) between the Andes and the lowlands of the Amazonian, Orinoquia and
Pacic regions were the areas where the greatest number of hotspots was concentrated. These results
provide valuable information on how better use ofcial institutional information to quickly dene and
prioritise ES, to guide management actions within the countrys recent policies on integrated water
resources management and on biodiversity and ES.
2014 Elsevier Ltd. All rights reserved.

Introduction (Daily and Matson, 2008; Farrell and Anderson, 2010; Kroll et al.,
2012).
The concept of ecosystem services (ES), dened as the benets In the past decade, many publications have synthesised discuss-
that human beings obtain from ecosystems (MA, 2005), has become ions around the ES concept and their classication system (de Groot
a key tool for different stakeholders interested in linking natural, et al., 2002; Wallace, 2007; Costanza, 2008; Braat and de Groot,
human and economic systems (Armsworth et al., 2007; Bryan et al., 2012), payment for ES (PES) (Van Hecken and Bastiaensen, 2010;
2010; Muradian and Rival, 2012). There is an increasing interest Wnscher and Engel, 2012) or the link between ecosystem pro-
in incorporating ES into environmental planning policies (de Groot cesses, biodiversity, climate change, land use and ES (Egoh et al.,
et al., 2010; Muradian and Rival, 2012; Viglizzo et al., 2012) and into 2007; Fu et al., 2012; Armstrong et al., 2012; Mace et al., 2012).
the design of objectives and strategies for landscape management, However, there is still a lack of information and empirical data
with the aim of improving the provision of these services to society on the distribution, service uxes and trade-offs between differ-
ent landscape functions and how these ES change over time and
across different spatial scales (de Groot et al., 2010; Haines-Young
et al., 2012; Mace et al., 2012).
Corresponding author at: Universidad Nacional de Colombia, Laboratorio de
One of the requirements to apply the ES concept and decision-
Ecologa del Paisaje y Modelacin de Ecosistemas. Carrera 30 No. 45-03, Edicio
making is the quantication and mapping of services (Braat and de
421, Of. 223, Bogot, D.C., Colombia. Tel.: +57 1 3165000x11333.
E-mail addresses: nrodrigueze@unal.edu.co, neraso2000@gmail.com Groot, 2012; Burkhard et al., 2012; Maes et al., 2012a). Mapping ES
(N. Rodrguez). is the initial step for the subsequent analyses of ecological, social

http://dx.doi.org/10.1016/j.landusepol.2014.09.013
0264-8377/ 2014 Elsevier Ltd. All rights reserved.
610 N. Rodrguez et al. / Land Use Policy 42 (2015) 609618

and economic processes associated with ES (TEEB, 2010). Both pro- often collected at different scales and are limited in its availability.
cesses help answer questions related to the state and trends of ES Currently, attention on ES is focused on tropical countries. We have
for society, the drivers that affect them and the priorities of conser- formulated the following questions: (1) What is the spatial distri-
vation and restoration strategies (Maes et al., 2012b). The mapping bution for ES? (2) To what extent are ES correlated on both national
and modelling methods are varied, depend on the research objec- and watershed levels? (3) What geographical areas maximise the
tives, type of service and working scale, and are still undergoing different ES production (i.e., what are the ES hotspots)? Using avail-
development and validation (Nedkov and Burkhard, 2012). The able public information related to water resources, forests, soils and
current trends in mapping and modelling include research on the use of geographic information tools, we have evaluated the fol-
biodiversity, species functions, habitat structure, ecosystem pro- lowing ve ES in Colombia: water provision, regulation of water
cesses, ecological production functions and landscape function ow, carbon storage in the above-ground biomass and in the soil
analyses (Lavorel and Grigulis, 2012; Maes et al., 2012a; Nedkov and nally landslide prevention.
and Burkhard, 2012; Bastian, 2013).
Generally, information on ES mapping and modelling focuses on
Methods
the distribution of services, especially food and water provision and
regulation (UNEP-WCMC, 2011), and the majority of this research
Study area
consists of studies conducted at different spatial scales (Maes et al.,
2012a). China, South Africa, USA, the Netherlands and Australia
Colombia is located in north-western South America and is con-
are the countries in which most of the research is conducted for
sidered to be a mega-diverse country, with 34 different biomes
this subject (Egoh et al., 2008, 2012; Costanza and Kubiszewski,
and 132 natural ecosystem types (IDEAM et al., 2007). The coun-
2012). Ecosystem functions, such as inputs for mapping, are gen-
try covers approximately 1,142,000 km2 in continental area and
erally linked through models or indicators from the primary data
has ve natural regions that are associated with 41 watersheds
by relating these functions to maps of land use/cover, eco-regions
(Fig. 1), which are used as units of analysis in this study: the Andean
or habitat maps (Burkhard et al., 2012; Haines-Young et al., 2012;
(including the three Andes ranges, the Inter-Andean valleys and
Maes et al., 2012b). The capacity of the ecosystem capacity to sup-
the Magdalena-Cauca watersheds), the Caribbean, the Amazonian,
ply certain ES and the actual usage by people varies considerably
the Pacic and the Orinoco. These regions have contrasting hydro-
(Bastian, 2013) because ecosystem functions depend mainly on bio-
climatic, geomorphologic, topographic, edaphic and land use/cover
physical conditions and land use (de Groot et al., 2010; Burkhard
conditions as well as different levels of socio-economic develop-
et al., 2012).
ment (Poveda et al., 2011; Armenteras-Pascual et al., 2011). The
In Latin America (LA), between the years 2001 and 2004, the Mil-
country is characterised by a high water yield with uvial dis-
lennium Ecosystem Assessment initiative catalysed the increase in
charge that varies from 100 mm per year into the Caribbean to over
studies related to ES. Chile, Costa Rica, Colombia, Per, Argentina
6000 mm per year into the Pacic. The water volume in Colombia
and Brazil have conducted sub-global evaluations (MA, 2005), with
is 2084 km3 , which is distributed in ve big hydrological regions
differences among the studies that reect each countrys con-
that are divided into the 41 aforementioned watersheds also used
text, needs and pressures regarding their natural resources. In the
as level of analysis and that are currently monitored (MADS, 2010).
region, studies have focused on quantifying carbon- and water-
The population density of the country is 40 people/km2 , distributed
related services, and the payment for ecosystem services (PES)
irregularly, with ca. 85% of the population concentrated in urban
has received considerable attention (Corbera et al., 2007; Pagiola
centres of the Andean region, with 3500 people/km2 , in contrast
et al., 2007; Quintero et al., 2009), but trade-offs analyses are scarce
with the southern and western parts of the country, with less than
(Balvanera et al., 2012). The review by Balvanera et al. (2012) on the
1 person/km2 (http://www.dane.gov.co). More than one-third of
state of knowledge on this subject is noteworthy, concluding that
the territory has been transformed, with the current predominant
there are imbalances in the focus of interest and information avail-
land use being agriculture, including pasture in the Andean and
ability for each country and that the diversity of ecosystems and
Caribbean regions, tropical humid forests in the Amazonian and
people in LA should be taken into consideration for interventions
Pacic regions and savannahs in the Orinoquia region. The natural
and future scenarios. However, most countries have ofcial infor-
ecosystems are diverse, and although forests covered approxi-
mation that can be the basis for a national inventory of their ES
mately 57 million hectares in 2005, deforestation rate has been
and prioritise ES conservation areas. In Colombia, research on ES is
estimated to be 273,334 ha per year between 2000 and 2005
limited, and with the exception of the rst evaluation of ES within
(Cabrera et al., 2011). Moreover, in the past decade Colombia
the MA (2005) study (Armenteras et al., 2005), current interest
has experienced a ve-fold increase in foreign investment, espe-
revolves around PES related to hydrological services and biodiver-
cially in mineral extraction (e.g., oil, carbon and gold) (Banco de la
sity and pastoral systems (Murgueitio et al., 2011; Moreno-Sanchez
Repblica, 2012), a trend that is foreseen to be maintained and to
et al., 2012). Studies focusing on mapping and trade-offs are also
affect some of the basic services for people because many of these
scarce in Colombia (but see Tallis et al., 2012). Recently, Colombia
projects are planned to be developed in high biodiversity areas that
has incorporated ES in its biodiversity policy (MADS, 2012), the
are strategic for the conservation of water resources. Large projects
actions of which should be based on the knowledge and availabil-
aiming to produce biofuels are also being developed, together with
ity of spatial information on the state and trends of the ecosystems
a continuous encroachment of forests due to the progression of the
and ES at different scales for decision-making.
agricultural frontier in the Amazonian and Orinoquia regions.
Herein, we present the rst national mapping of ES in Colombia,
which is a country with high geographic heterogeneity and several
sources of environmental information that are often underused by Methods and databases used to estimate the ES
decision makers. The general objective of this study is to carry out
an evaluation of ecosystem services in Colombia for setting pri- We evaluated the spatial distribution of ve ES: water provi-
orities and planning carbon and water resource management. We sion, regulation of water ow, carbon storage in the above-ground
have based this study on two levels of analysis: ve natural regions biomass and carbon in the soil, and landslide prevention. These ES
and 41 watersheds. The study is interesting because it shows the were selected because of their relevance to environmental manage-
suitability of using available ofcial information and how to use it ment and planning and also for the availability of their data for the
as a surrogate to quickly map ES in tropical countries where data are whole country. Our approach uses the hierarchical classication of
N. Rodrguez et al. / Land Use Policy 42 (2015) 609618 611

Fig. 1. Map locating the study area including watershed boundaries.

ES proposed by The Economics of Ecosystems and Biodiversity ini- annual conditions (IDEAM, 2010). This map provided data at a
tiative (TEEB) (de Groot et al., 2010; UNEP-WCMC, 2011). According spatial resolution of 2 km and represented the supercial water
to this classication, the categories used were provisioning (water) quantity per unit catchment surface area for a certain time scale
and regulating (regulation of water ow, climate regulation includ- (runoff = precipitation real evapotranspiration). The range was
ing carbon storage and moderation of extreme events including 0.1737318.922 L/s km2 .
landslide prevention) (Table 1).

Water provision (WP)


The provision of fresh water has been identied as a funda- Regulation of water ow (RWF)
mental and non-replaceable service for human well-being, food RWF refers to the inuence of natural systems on the hydrologi-
production and economic development, as well as for the main- cal uxes at the surface of the Earth (Egoh et al., 2008) and includes
tenance of biodiversity (de Groot et al., 2002, 2010; Pert et al., processes associated with irrigation maintenance, natural drainage
2010; Nedkov and Burkhard, 2012). Additionally, the economies of and buffering stream ow extremes (de Groot et al., 2002). We
many sectors, such as agriculture, industry and tourism, depend used the information of the retention and hydrological regulation
on this service (Van Jaarsveld et al., 2005; Naidoo et al., 2008). index IRH (IDEAM, 2010) at a 2-km spatial resolution. This index
This service is highly dependent on the quantity and distribution (IRH = Vp/Vt) was estimated from the relationship between the area
of precipitation combined with a series of abiotic factors, such as below the mean ow line (Vp), and the corresponding area below
regional climatic systems and topography (de Groot et al., 2002). the daily ow duration curve (Vt), and its range was 0.390.89. It
We used a map of the water yield of Colombia for the mean is an adimensional index.
612 N. Rodrguez et al. / Land Use Policy 42 (2015) 609618

Table 1
Summary of the ecosystem services considered and dataset sources.

Service category Service types Biophysical component or process State indicator Range of value of Source
service

Provisioning Water provision The hydrologic cycle (precipitation, Water availability 0.1737318.922 L/s km2 National Water Study
evapotranspiration, vegetation, soil (L/s km2 ) (IDEAM, 2010)
and plant-available water content)
Regulating Regulation of water Role of forests in water inltration Water retention 0.390.89 National Water Study
ows and gradual release of water Index (IDEAM, 2010)
Climate regulation Inuence of ecosystems on local Above-ground 3.5147.5 tC/ha Map of carbon stored in
carbon storage in and global climate. Capacity that biomass (t/ha) above-ground biomass in
above-ground different land covers have to xate the forest of Colombia
biomass carbon in their structures (Phillips et al., 2011), Land
Use Changes (19702020)
and the Carbon Emissions
in the Colombian Llanos
(Etter et al., 2011)
Climate regulation Represents the process of soil % Soil organic <1.0% to >6.0% Report from Colombia.
carbon storage in formation linked to the carbon United Nations Framework
soil accumulation of organic matter Convention on Climate
Inuence of climate, soil type and Change (UNFCC), (IDEAM,
geomorphology 2001)
Landslide Role of vegetation has for slowing Landslide 5 categories: 0 The National landslide
prevention down the process of land susceptibility (very low) to 5 susceptibility map (IDEAM,
degradation through soil retention (very high) 2010)
Depends of topography,
geomorphology, soil and land
cover characteristics

Landslide prevention (LP) for each soil unit of the country (IDEAM, 2001). The map scale was
This factor refers to the capacity that vegetation has for slowing 1:500,000 and the values ranged from <0.1% to >6%.
down the process of land degradation through soil retention, and it
evaluates the function of vegetation cover and erosion ability (Egoh Land cover map
et al., 2008). We used the national landslide susceptibility map as
a proxy to evaluate this service (Snchez et al., 2010). This map We used a land cover map as a basis for quantifying and map-
analysed geological, geomorphologic and edaphic variables and ping ES, which is an appropriate approach for the national level
vegetation cover, identifying areas that should be managed for haz- and the data availability (Haines-Young et al., 2012). We also con-
ard prevention in the face of erosion and mass wasting processes sidered regions and watersheds as the central levels for analyses.
(LP = 0.15L + 0.15Df + 0.1Tm + 0.1Dd + 0.1S + 0.15P + 0.15Ie + 0.1Cv/Np, In particular, we used the CORINE land cover map for 20052009
where L is the lithology, Df is the density of fracturing, Tm is the (scale of 1:100,000) that, for Colombia, was based on the inter-
morphology, Dd is the drainage density, S is the soil, P is the slope, pretation of Landsat and Spot satellite images and on validation
Ie is the intensity of erosion, Cv is the land cover and Np is the in the eld (IDEAM et al., 2012). For the purposes of the present
number of parameters). In accordance with expert criterion, ve study, we focused on continental covers using the second hier-
degrees of susceptibility were established for this map: null, low, archical level that has 14 cover classes: urban fabric; industrial;
medium, high and very high; the map scale was 1:500,000. commercial and transportation; mine, dumping and construction
sites; articial non-agricultural vegetated areas; arable land; per-
manent crops; pastures; heterogeneous agricultural areas; forest,
Carbon storage in the above-ground biomass (CAGB)
shrub and/or herbaceous vegetation associations; open spaces with
This factor refers to the capacity that different land covers have
little or no vegetation; inland wetlands; coastal wetlands; and
to x carbon in their structures and remove CO2 from the atmo-
inland waters. For the forest category, we used a map of the above-
sphere, which contributes to climate change (Bai et al., 2011). For
ground biomass (AGB) (Phillips et al., 2011), the map was created
the forest category, we used a map of above-ground biomass (AGB).
from the forest/non-forest map from the national REDD Project
The estimates were realised for 16 types of natural forest using allo-
combined with stratication of 16 natural forest types. The maps
metric models of AGB (Phillips et al., 2011; Alvarez et al., 2012), with
have a spatial resolution at 270 m.
biomass ranging from 96.2 t/ha to 295.1 t/ha. The carbon-fraction is
calculated by conversion factor of 0.5 AGB. For shrub and/or herba-
ceous vegetation, we used values provided in the literature (IDEAM, ES mapping
2009; Etter et al., 2011), and for the rest of the land cover types, we
used estimates reported for Colombia by Yepes et al. (2011). The One of the simplest methods for general ES mapping is to com-
map has a spatial resolution of 270 m. bine resource availability with an assessment of the vegetation
associated with availability as a proxy for assessing the presence of
ES rather than the service. This approach has been applied in other
Carbon storage in the soil (SoilC) regions (Egoh et al., 2008, 2009) and has been frequently used to
This factor represents the process of soil formation linked to map ES when data availability is limited and the focus is on the
the accumulation of organic matter (Egoh et al., 2008). The map of presence of ES (Maes et al., 2012a). In this study we also used this
organic carbon distribution in Colombian soils was used, which was approach given the fact that different land covers generate a gradi-
based on the work on soils by the Agustn Codazzi Geographic Insti- ent of conditions in terms of structures and processes necessary to
tute (Instituto Geograco Agustn Codazzi), modied by the IDEAM. provide ecosystem services and thus dene the potential of deliv-
This map incorporated information on geomorphology, climate, ering them (Maes et al., 2012b). We also assumed not only that
physical and chemical soil properties and soil taxonomic classes natural ecosystems had good capacities to supply ES but also that as
N. Rodrguez et al. / Land Use Policy 42 (2015) 609618 613

Table 2 a total of 11,537 cells) using the geographic information system GIS
Weights assigned to ecosystem services in relation with the different land cover
package ArcGIS 10.1 (ESRI) for spatial analyses. Each cell value rep-
classes. A value 0 = no relevant capacity to supply services and a value 1 = highest
capacity to supply services. resented the ecosystem service value (an average weighted value
calculated using Spatial Analyst in ArcMap 10 (ESRI)) with respect
CLC classes RWF WP LP SoilC
to the land cover type and the area of the cell. We identied hotspots
Urban fabric 0 0 0 0 for each service using the following denition of hotspot: an area
Industrial, commercial and 0 0 0 0 that provides large components of a particular service and the
transportation
criteria proposed by Bai et al. (2011), i.e., the richest 10% of grid
Mine, dump and construction sites 0 0 0 0
Articial non-agricultural 0.2 0.2 0.2 0.2 cells, to obtain the hotspot maps. With a superposition process
vegetated areas using individual maps, we obtained a total hotspot map.
Arable land 0.2 0.2 0.4 0.2 The relationships between pairs of ES at the watershed (41
Permanent crops 0.6 0.6 0.6 0.6
cases) and national (11,537 quadrats) levels were conducted using
Pasture 0.5 0.6 0.4 0.4
Heterogeneous agricultural areas 0.6 0.6 0.6 0.5 Pearson correlation analyses. Two variables, CAGB and FM, were
Forest 1 1 1 1 square root-transformed prior to these analyses to reach normality.
Shrub and/or herbaceous 1 1 1 1 A principal component analysis (PCA) was performed to evaluate
vegetation associations the relationship among the different ES using the values from the
Open spaces with little or no 0 0 0.2 0.2
41 watersheds. The objective of this analysis was to reduce the
vegetation
Inland wetlands 1 1 1 1 number of variables and generate new axes that best explained the
Coastal wetlands 1 1 1 1 variance in the data and illustrated the relationship among the ES.
Inland waters 1 1 1 1 The STATISTICA (StatSoft, 2001) software was used for all statistical
Indicator values assigned to every land cover class: regulation of water ow (RWF), analyses.
landslide prevention (LP) derived from literature (Burkhard et al., 2012; Nedkov and
Burkhard, 2012; Koschke et al., 2012). Water provision (WP) and carbon storage in
the soil (SoilC) derived from expert criteria. For carbon storage in above-ground Results
biomass (CAGB) the values of ecosystems services were reported of Colombia.

The results show that there were differences in the spatial distri-
the extent of human impact increased, the services supply capacity bution of the ES among regions and that each region was associated
of the land cover varied strongly and tended to decrease (de Groot with maximising the supply of one or two ES. In general, the coun-
et al., 2010; Haines-Young et al., 2012). We dened a scale ranging try had high mean values of water yield (62.5 L/s km2 ) and CAGB
from 0 to 1 to relate each service studied here with the different (69.3 tC/ha). The Pacic and Amazonian regions present the high-
land cover types based on previous studies of the ES that regulate est mean values for the services of water provision (125.8 and
water ow and prevent landslides (Burkhard et al., 2012; Nedkov 71.9 L/s km2 , respectively), regulation of water ow (>0.72 for both)
and Burkhard, 2012; Koschke et al., 2012). We also used expert and CAGB (60.3 and 120.9 t/ha, respectively), with the Caquet,
local knowledge to generate consistent values for water provision Putumayo and Amazonas-direct watersheds standing out the most;
and carbon storage in the soil. A consensus was reached after three the Andean region was important for LP (>2.5) and maintaining the
expert workshops with national experts on hydrology, soils and percentage of carbon in the soil (>0.03%) (Table 3). The ecosystems
environmental issues (Table 2). A value of 0 indicates that there is from the Orinoquia region present medium value for landslide pre-
no relevant capacity to supply services, and a value of 1 indicates the vention, whereas the Caribbean region presented low values for all
highest capacity to supply these services. We generated a map for ES (Table 3). At the watershed level, all the watersheds from the
each ecosystem service by multiplying the original value from the Amazonian region stood out with the highest mean values for ser-
services dataset by the value given as a function of the land cover vices related to water and CAGB, and the Apure (Orinoquia), San
type (from 0 i.e., land cover not relevant for a service to 1 i.e., max- Juan and Pacic-direct (Pacic) watersheds were important for the
imum contribution by a specic cover to maintain a service). The services of soil organic carbon and LP. Fig. 2 illustrates the distri-
ecosystem service maps were rasterised and converted to a 270 m bution of the ve services studied, indicating the range of values
spatial resolution. As explained above, the CAGB map was a gener- at the national scale. The highest values for the regulation of water
ated as combination of available biomass and carbon information ow service (>0.53) are distributed irregularly across the majority
for the entire country (Phillips et al., 2011). of the country (except for the Caribbean and Orinoquia regions)
(Fig. 2A), and the highest values for water provision (>90 L/s km2 )
Analysis were found in most of the Pacic region and in the upper Ro
Caquet and Putumayo watersheds (Amazonian region) (Fig. 2B).
To generated results that can be used at different planning levels, The areas with the highest values for Landslide prevention (<3.7%)
we evaluated the ES using two analyses levels: (i) the ve natural corresponded to the boundary (piedmont) of the Andean region
regions of the country and (ii) the 41 watersheds. To facilitate the with the lowlands (Fig. 2C), mainly the upper parts of the Caquet,
statistical analyses, we divided the country into 10 10 km grid (for Putumayo, Guaviare (Amazonas), Meta, Casanare (Orinoquia), San

Table 3
Average values for six ecosystem services studied at the regional scale and percentage of each ecosystem service hotspot within the region.

Region RWF WP LP CAGB SoilC

Mean % Hotspot Mean % Hotspot Mean % Hotspot Mean % Hotspot Mean % Hotspot

Caribbean 0.4 6.1 21.1 0.0 1.3 7.67 21.1 2.6 0.01 0.6
Pacic 0.7 7.7 125.8 76.2 2.2 5.79 60.4 1.6 0.02 13.2
Andes 0.5 18.8 43.6 23.8 2.53 54.8 39.5 5.9 0.03 84.9
Orinoco 0.5 16.0 46.6 0.0 2.59 30.8 28.4 6.6 0.01 0.5
Amazon 0.7 51.4 71.9 0.0 1.58 1.0 120.9 83.3 0.01 0.8
National average 0.59 62.45 1.76 69.3 0.02

Regulation of water ow (RWF), Water provision (WP), Landslide prevention (LP), Carbon storage in above-ground biomass (CAGB) and Carbon storage in the soil (SoilC).
614 N. Rodrguez et al. / Land Use Policy 42 (2015) 609618

Fig. 2. Distribution spatial of the ve ecosystem services, indicating the range of values at the national scale. The black represents the hotspots.

Jun and Micay-direct (Pacic) watersheds. Important areas in Between 39% and 43% of the countrys area contained hotspots
terms of CAGB were identied, with the exception of the Amazo- associated with the RWF and carbon CAGB, respectively. These ser-
nian region, as some areas of the Andes (values >132.05 tC/ha) that vices were concentrated in the Pacic and Amazonian regions. The
coincided with forest ecosystems within the National Park System remaining ES have a lower area hotspots (<16%), where the hotspots
of Colombia (Fig. 2D). Finally, the highest values for the service of corresponding to water provisions occupied the lower percentage
carbon storage in the soil (>0.66%) were limited to the Andes and (<1%), even though the mean values for this service were high across
some areas of the Pacic region (Fig. 2E). the country. The Andean region contained approximately 85% of
N. Rodrguez et al. / Land Use Policy 42 (2015) 609618 615

Fig. 3. Map of ecosystem services hotspots overlap. Shown the number of overlapping ecosystem services in an analysis levels.

the hotspots corresponding to soil carbon content, and 85% of the


LP hotspot was concentrated in these two regions. The Caribbean
region had the lowest percentage of hotspot area (Table 3). For the
case of the superposition of different hotspots for Colombia, we
found that approximately 33% of the areas had no hotspots, 15.8%
Table 4
had one hotspot and approximately 46% contained areas where Correlation between the different ecosystems services (A) national scale and (B)
two ES converge (Fig. 3). The latter areas were mainly located in watersheds scale. Values in bold indicate signicance (p < 0.01).
the watersheds of the Amazonian and Pacic regions, where the ES
RWF WP LP CAGB SoilC
of water provision, RWF and CAGB were correlated. Areas where
(A) National scale
four ES were superimposed were scarce (less than 1% of the coun-
RWF 1
try) and were located in the Andean (Alto Magdalena and Saldana WP 0.74 1
watersheds) and Pacic (San Jun and Mira watersheds) regions. LP 0.13 0.19 1
The correlation between the different services was variable CAGB 0.64 0.78 0.10 1
(Table 4A and B), and higher correlations were found when the CSUELO 0.05 0.12 0.39 0.02 1
(B) Watersheds scale
analysis was conducted at the national level. In general, we found
RWF 1
that the highest correlations were between the ES of regulation of WP 0.92 1
water ow and CAGB and between the former and water provision, LP 0.25 0.27 1
with higher correlation values at the watershed level (Table 4A and CAGB 0.77 0.85 0.07 1
CSUELO 0.15 0.28 0.58 0.03 1
B). Notably at the country level, the landslide prevention ES showed
616 N. Rodrguez et al. / Land Use Policy 42 (2015) 609618

Fig. 4. Principal Component Analyses at regional and watershed levels.

a positive correlation with all ES. At the watershed scale, soil carbon (IAvH et al., 2011), and the CAGB for 2010 was estimated to be
was related positively to LP. 7,144,861,815 tC (Yepes et al., 2011).
The PCA conducted to establish joint relationships among all ES There are differences in the distribution and values of the ES
showed that the rst two components explained approximately analysed that reect, on the one hand, the natural capacity of the
86% of the variance and a very clear distribution of the water- different ecosystems to supply services with particular hydrologic,
sheds in the plane according to the natural regions to which they climatic, topographic, edaphic and land cover conditions. On the
belonged. According to axis I (57.4% of the variance explained), we other hand, these differences also reect the degree of transfor-
separated the watersheds belonging to the Amazonian and Pacic mation in many regions, where the capacity to supply or regulate
regions in the right corner of the axis, those from the Andean and the analysed services is decreasing and other services, such as crop
Orinoquia regions towards the centre and those from the Caribbean production, are relevant. This is the case of the Caribbean region
region to the left. The right side of axis I is characterised by high val- and part of the Andean region. This nding is in accordance with
ues for CAGB, WRF and water provision (Fig. 4). According to axis II, the hypotheses of Braat and Brink (2008), Haines-Young (2009) and
we separated watersheds from the Pacic and Andean regions into de Groot et al. (2010), who suggested that land use is a key factor
the upper section and watersheds from the Amazonian and Orino- in the loss of certain ES and that the gradient and intensity of use
quia regions and, to lesser extent, those from the Caribbean region would favour other ES.
into the lower section. This separation was performed because high The supply pattern of the CAGB and RWF services reects the
values of soil carbon and landslides were found in the upper section distribution of forest ecosystems in the country, concentrating, as
of the axis. In general terms, for the ES considered in this study, the expected, in the Amazonian and Pacic regions and more sparsely
country could be divided into three groups: Group I would consist in areas of the Andean region where some National Parks are
of watersheds from the Amazonian region, where the services of located (such as Paramillo and Sierra Nevada de Santa Marta).
CAGB, RWF and water provision were maximised; Group II con- The spatial distribution of these services, particularly carbon, is in
tained the watersheds from the Pacic and some from the Andean accordance with the ndings at the global scale by Naidoo et al.
regions, where the maximised ES were landslide prevention and (2008) and, at the country level, by Tallis et al. (2012), who also
soil carbon; and Group III would consist of the watersheds from reported low values of carbon to the west of the Andes and for
the Orinoquia and Caribbean and some from the Andean regions, the Caribbean region, relating these values to population density.
which have no specic associated ES. The watersheds from the Pacic region and those with headwaters
in the Andes and that drain to the Amazon and Orinoquia rivers
Discussion have large water provision values. This may be associated with the
incidence of hydroclimatic conditions originated by atmospheric
Colombia plays an important role at the regional level for the circulation patterns from the Pacic Ocean and Caribbean Sea, the
supply of ES related to water and carbon due to its geographic, dynamic hydroclimatic systems from the Amazonian and Orino-
topographic and hydroclimatic characteristics (Poveda et al., 2011) quia regions and topographic gradients (Poveda et al., 2011). The
and because more than 50% of the territory is covered by tropical IDEAM (2010) reported that these areas were considered to have
forests. The total water yield of the country (63 L/s km2 ) exceeds the the highest water yields and to be providers of water for the coun-
mean global water yield (10 L/s km2 ) by approximately six times try (ca. 70%) and that many of the streams are direct tributaries
N. Rodrguez et al. / Land Use Policy 42 (2015) 609618 617

of the Amazon and Orinoco Rivers, responsible for the majority of consequences of different policy scenarios related to land use
the water in South America (Restrepo et al., 2006). In contrast, the change, mining and large-scale agro-industrial developments cur-
Caribbean region presents low values for ES associated with water rently being a hot topic in the country. Following the same trend,
resources and is vulnerable to water shortages (IDEAM, 2010), with the watershed level results of our study may guide the imple-
the associated social implications of such shortages. mentation of the current very comprehensive policy on water
The piedmont areas and the Andean slopes, which are covered resources management. Indeed our results give support to the pri-
generally with forests, are important for the service of landslide oritisation for watershed management in the country that has yet
prevention, and their spatial distribution coincides with that given to be dened.
in the work by Tallis et al. (2012). However, there are low to inter- Thus, the grouping of watersheds as a function of the services
mediate values for this service in the upper and mid-altitude areas they supply may be used as a basis for environmental planning.
of the watersheds that drain to the Orinoco and Amazon rivers Similarly, the fact that important areas for supply coincide with
and for watersheds that drain to the mid-section of the Magdalena protected areas may be considered to be a winwin situation
River. These watersheds, similar to other tropical mountain zones among conservation and ES and to present opportunities to revise
of South America, are particularly sensitive to erosion, landslides Colombias conservation priorities.
(Vanacker et al., 2005) and excessive sediment transport (Restrepo
et al., 2006; Molina et al., 2008). This is in part due to steep topo-
Acknowledgments
graphic gradients, high precipitation, land use changes and poor
agricultural management practices. The Andean region also con-
The authors would like to acknowledge the support of the
centrates the highest values of ES associated with soil carbon,
Institute of Hydrology, Meteorology and Environmental Studies
particularly the central mountain range, and this association may
(IDEAM) and the Geographic Institute Agustn Codazzi (IGAC) for
be related to the soil type, which is generally derived from volcanic
facilitating access to the data used in the present study. We also
ash, the climatic conditions and the lithology.
acknowledge the collaboration of Luz Marina Arvalo, director of
The analysed ES showed a positive correlation in both analysis
Ecosystems and Environmental Data within the IDEAM and all the
levels, such as among the ES of water provision, RWF and CAGB
professionals working under this section and the Hydrology section
(r > 0.74), presenting a spatial overlap in the low areas of the Ama-
of the IDEAM in the establishment of the criteria to evaluate the ES.
zonian and Pacic regions and reecting in part the distribution
We thank the Vice-Rector of Research from the National University
of the lowland forest ecosystems of the country. It is the advis-
of Colombia for funding the study through the postdoctoral posi-
able and possible to guarantee the permanence of these three ES
tion of Nelly Rodrguez and Research Groups Strengthening Grants
with national and regional policies aimed at reducing deforesta-
and Carol Franco for her help with the graphics. We also thank the
tion and with planning tools such as the declaration of gures
CYTED network IBEROREDD+ for nancial support of the research.
of protection at the regional scale. This correlation contrasts with
the negative relationship observed and the lack of spatial overlap
between the ES of LP (Andean), explained by the topographic gra- References
dient. The additional insight provided by the PCA corroborated the
type of correlations showing that the ES may be grouped for their Alvarez, E., Duque, A., Saldarriaga, J., Cabrera, K., de las Salas, G., del Valle, I., Lema, A.,
Moreno, F., Orrego, S., Rodrguez, L., 2012. Tree above-ground biomass allome-
management into three groups, where various services concur- tries for carbon stocks estimation in the natural forests of Colombia. Forest Ecol.
rently occur spatially in one region and watershed, thereby guiding Manag. 267, 297308.
both ecosystem conservation and restoration actions. Armenteras, D., Rincn, A., Ortiz, N., 2005. Ecological Function Assessment in the
Colombian Andean Coffee-growing Region, Sub-global Assessment Report. Mil-
The high degree of spatial overlap between hotspots for the lennium Ecosystem Assessment.
three ES that were correlated most strongly (WP, RFW and CAGB) Armenteras-Pascual, D., Retana-Alumbreros, J., Molowny-Horas, R., Roman-Cuesta,
and the low overlap between the hotspots for more than four ES R.M., Gonzalez-Alonso, F., Morales-Rivas, M., 2011. Characterising re spatial
pattern interactions with climate and vegetation in Colombia. Agric. Forest
(<1% of the country) suggest particular management strategies. The Meteorol. 151, 279289.
protection of areas with a high number of hotspots, such as tran- Armstrong, C.W., Foley, N.S., Tinch, R., Van den Hove, S., 2012. Services from the
sition areas (piedmonts) between the Andes and lowlands of the deep: steps towards valuation of deep sea goods and services. Ecosyst. Serv. 2,
213.
Amazonian, Orinoquia and Pacic regions and some areas of the
Armsworth, P.R., Chan, K.M., Daily, G.C., Ehrlich, P.R., Kremen, C., Ricketts, T.H.,
Andean region (e.g., Colombian Massif and mountain tops), would Sanjayan, M., 2007. Ecosystem-service science and the way forward for con-
be the most efcient and urgent management option. These areas servation. Conserv. Biol. 21, 13831384.
have high ecosystem diversity and landscapes critical to the nat- Bai, Y., Zhuang, C., Ouyang, Z., Zheng, H., Jiang, B., 2011. Spatial characteristics
between biodiversity and ecosystem services in a human-dominated watershed.
ural supply of ES but, at the same time, have been identied as Ecol. Complex. 8, 177183.
hotspots for deforestation; under scenarios of land use change, Balvanera, P., Uriarte, M., Almeida-Lenero, L., Altesor, A., Declerck, F., Gardner, T.,
these areas may reduce the supply of important ES, such as bio- Hall, J., Lara, A., Laterra, P., et al., 2012. Ecosystem services research in Latin
America: the state of the art. Ecosyst. Serv. 2, 5670.
diversity and water and climate regulation (Rodrguez Eraso et al., Banco de la Repblica, 2012. Informe de la Junta directiva al Congreso de La Repblica
2012), and hydrological functioning may be affected in processes , Bogot, DC.
such as stream ow, evapotranspiration and inltration (Molina Bastian, O., 2013. The role of biodiversity in supporting ecosystem services in Natura
2000 sites. Ecol. Indic. 24, 1222.
et al., 2012). Nevertheless, regions such as the Orinoco and the Braat, L., ten Brink, P. (Eds.), 2008. The Cost of Policy Inaction. The Case of Not
Caribbean should be evaluated with another set of ES, as those Meeting the 2010 Biodiversity Target. Study for the European Commission, DG
related to ood control, where likely they will present the highest Environment, Wageningen.
Braat, L.C., de Groot, R.S., 2012. The ecosystem services agenda: bridging the worlds
values. of natural science and economics, conservation and development, and public
Finally and despite some of the limitations raised above, our and private policy. Ecosyst. Serv. 1, 415.
study contributes to the identication and synergies of the most Bryan, B., Grandgirard, A., Ward, J.R., 2010. Quantifying and exploring strategic
regional priorities for managing natural capital and ecosystem services given
important areas for the conservation of ES using available national
multiple stakeholder perspectives. Ecosystems 13, 539555.
information. These results could be incorporated during the imple- Burkhard, B., Kroll, F., Nedkov, S., Mller, F., 2012. Mapping ecosystem service supply,
mentation of national policies such as the National Policy for the demand and budgets. Ecol. Indic. 21, 1729.
Management of Biodiversity and Ecosystem Services or future Cabrera, E., Vargas, D.M., Galindo, G., Garca, M.C., 2011. Memoria Tcnica: Cuan-
ticacin de la tasa de Deforestacin para Colombia, Periodo 19902000,
Reducing emissions from deforestation and forest degradation 20002005. Instituto de Hidrologa, Meteorologa y Estudios Ambientales
related policies. Further these results can help assess the spatial IDEAM, Bogot, DC.
618 N. Rodrguez et al. / Land Use Policy 42 (2015) 609618

Corbera, E., Kosoy, N., Martinez, M., 2007. Equity implications of marketing ecosys- Molina, A., Govers, G., Poesen, J., Van Hemelryck, H., De Bivre, B., Vanacker, V., 2008.
tem services in protected areas and rural communities: case studies from Environmental factors controlling spatial variation in sediment yield in a central
Meso-America. Global Environ. Change 17, 365380. Andean mountain area. Geomorphology 98, 176186.
Costanza, R., 2008. Ecosystem services: multiple classication systems are needed. Molina, A., Vanacker, V., Balthazar, V., Mora, D., Govers, G., 2012. Complex land cover
Biol. Conserv. 141, 350352. change, water and sediment yield in a degraded Andean environment. J. Hydrol.
Costanza, R., Kubiszewski, I., 2012. The authorship structure of ecosystem services 472473, 2535.
as a transdisciplinary eld of scholarship. Ecosyst. Serv. 1, 1625. Moreno-Sanchez, R., Maldonado, J.H., Wunder, S., Borda-Almanza, C., 2012. Hetero-
Daily, G.C., Matson, P., 2008. Ecosystem services: from theory to implementation. geneous users and willingness to pay in an ongoing payment for watershed
Proc. Natl. Acad. Sci. U. S. A. 105, 94559456. protection initiative in the Colombian Andes. Ecol. Econ. 75, 126134.
de Groot, R.S., Wilson, M., Boumans, R.M., 2002. A typology for the classication, Muradian, R., Rival, L., 2012. Between markets and hierarchies: the challenge of
description and valuation of ecosystem functions, goods and services. Ecol. Econ. governing ecosystem services. Ecosyst. Serv. 1, 93100.
41, 393408. Murgueitio, E., Calle, Z., Uribe, F., Calle, A., Solorio, B., 2011. Native trees and shrubs
de Groot, R.S., Alkemade, R., Braat, L., Hein, L., Willemen, L., 2010. Challenges in for the productive rehabilitation of tropical cattle ranching lands. Forest Ecol.
integrating the concept of ecosystem services and values in landscape planning, Manag. 261, 16541663.
management and decision making. Ecol. Complex. 7, 260272. Naidoo, R., Balmford, A., Costanza, R., Fisher, B., Green, R.E., Lehner, B., Malcolm, T.R.,
Egoh, B., Rouget, M., Reyers, B., Knight, A.T., Cowling, R.M., Van Jaarsveld, A.S., Ricketts, T.H., 2008. Global mapping of ecosystem services and conservation
Welz, A., 2007. Integrating ecosystem services into conservation assessments: priorities. Proc. Natl. Acad. Sci. U. S. A. 105, 94959500.
a review. Ecol. Econ. 63, 714721. Nedkov, S., Burkhard, B., 2012. Flood regulating ecosystem services mapping
Egoh, B., Reyers, B., Rouget, M., Richardson, D.M., Le Maitre, D.C., van Jaarsveld, supply and demand, in the Etropole municipality, Bulgaria. Ecol. Indic. 21,
A.S., 2008. Mapping ecosystem services for planning and management. Agric. 6779.
Ecosyst. Environ. 127, 135140. Pagiola, S., Ramrez, E., Gobbi, J., Haan, C., Ibrahim, M., Murgueitio, E., Ruz, J.P., 2007.
Egoh, B., Reyers, B., Rouget, M., Rouget, M., Richardson, D.M., 2009. Spatial congru- Paying for the environmental services of silvopastoral practices in Nicaragua.
ence between biodiversity and ecosystem services in South Africa. Biol. Conserv. Ecol. Econ. 64, 374385.
142, 553562. Pert, P.L., Butler, J.R., Brodie, J.E., Bruce, C., Honzk, M., Kroon, F.J., Metcalfe, D.,
Egoh, B., OFarrell, P.J., Charef, A., Gurney, L.J., Koellner, T., Nibam Abi, H., Ego, M., Mitchell, D., Wong, G., 2010. A catchment-based approach to mapping hydro-
Willemen, L., 2012. An African account of ecosystem service provision: use, logical ecosystem services using riparian habitat: a case study from the Wet
threats and policy options for sustainable livelihoods. Ecosyst. Serv. 2, 7181. Tropics, Australia. Ecol. Complex. 7, 378388.
Etter, A., Sarmiento, A., Romero, M., 2011. Land use changes (19702020) and the car- Phillips, J.F., Duque, A.J., Yepes, A.P., Cabrera, K.R., Garca, M.C., Navarrete, D.A.,
bon emissions in the Colombian Llanos. In: Hill, J.M., Hanan, N.P. (Eds.), Ecosys- lvarez, E., Crdenas, D., 2011. Estimacin de las reservas actuales (2010) de
tem Function in Savannas: Measurement and Modeling at Landscape to Global carbono almacenadas en la biomasa area en bosques naturales de Colombia.
Scales. Taylor & Francis, CRC Press, pp. 383402, http://www.crcpress.com/ Estraticacin, alometra y mtodos anliticos. Instituto de Hidrologa, Meteo-
product/isbn/9781439804704 rologa, y Estudios Ambientales, Bogot, DC.
Farrell, P.J.O., Anderson, P.M.L., 2010. Sustainable multifunctional landscapes: a Poveda, G., lvarez, D.M., Rueda, ., 2011. Hydro-climatic variability over the Andes
review to implementation. Curr. Opin. Environ. Sustain. 2, 5965. of Colombia associated with ENSO: a review of climatic processes and their
Fu, B., Wang, S., Su, C., Forsius, M., 2012. Linking ecosystem processes and ecosystem impact on one of the Earths most important biodiversity hotspots. Clim. Dyn.
services. Curr. Opin. Environ. Sustain. 5, 17. 36, 22332249.
Haines-Young, R., 2009. Land use and biodiversity relationships. Land Use Policy Quintero, M., Wunder, S., Estrada, R.D., 2009. Forest ecology and management for
26S, 178186. services rendered? Modeling hydrology and livelihoods in Andean payments for
Haines-Young, R., Potschin, M., Kienast, F., 2012. Indicators of ecosystem service environmental services schemes. Forest Ecol. Manag. 258, 18711880.
potential at European scales: mapping marginal changes and trade-offs. Ecol. Restrepo, J.D., Kjerfve, B., Hermelin, M., Restrepo, J.C., 2006. Factors controlling sed-
Indic. 21, 3953. iment yield in a major South American drainage basin: the Magdalena River,
IAvH, IDEAM, IIAP, INVEMAR, SINCHI, 2011. Informe del Estado del Medio Ambiente Colombia. J. Hydrol. 316, 213232.
y de los Recursos Naturales Renovables 2010. Instituto de Hidrologa, Meteo- Rodrguez Eraso, N., Armenteras-Pascual, D., Retana Alumbreros, J., 2012. Land use
rologa y Estudios Ambientales IDEAM, Bogot, DC. and land cover change in the Colombian Andes: dynamics and future scenarios.
IDEAM, IGAC, IAvH, INVEMAR, SINCHI, IIAP, 2007. Ecosistemas continentales, cos- J. Land Use Sci., 121, http://dx.doi.org/10.1080/1747423X.2011.650228.
teros y marinos de Colombia. Bogot DC. Snchez, R., Urrego, L., Mayorga, R., Vargas, G., 2010. Metodologa para la zonicacin
IDEAM, 2001. Mapa de la distribucin del carbono orgnico en los suelos de de susceptibilidad general del terreno a los movimientos en masa. Instituto de
Colombia. Instituto de Hidrologa, Meteorologa y Estudios Ambientales, Bogot, Hidrologa, Meteorologa, y Estudios Ambientales, Bogot, DC.
DC. StatSoft, Inc., 2001. STATISTICA for Windows. StatSoft, Inc, Tulsa, OK.
IDEAM, 2009. Caracterizacin preliminar del ciclo del carbono a partir de la infor- Tallis, H., Polasky, S., Lozano, J.S., Wolny, S., 2012. Inclusive wealth accounting for reg-
macin existente. Quinto Informe. Proyecto Piloto Nacional de Adaptacin al ulating ecosystem services. In: UNU-IHDP, UNEP (Eds.), Inclusive Wealth Report
Cambio ClimticoINAP. Componente B- Alta Montana. Instituto de Hidrologa, 2012. Measuring Progress Towards Sustainability. Cambridge University Press,
Meteorologa y Estudios Ambientales, Bogot, DC. http://www.unep.org/pdf/IWR 2012.pdf
IDEAM, 2010. Estudio Nacional del Agua. Instituto de Hidrologa, Meteorologa y TEEB, 2010. In: Kumar, P. (Ed.), The Economics of Ecosystems and Biodiversity. The
Estudios Ambientales, Bogot, DC. Ecological and Economic Foundations, London.
IDEAM, MADS, IGAC, IIAP, SINCHI, PNN, 2012. Capa Nacional de Cobertura de la UNEP-WCMC, 2011. Developing Ecosystem Service Indicators: Experiences and
Tierra (periodo 20052009): Metodologa CORINE Land Cover adaptada para Lessons Learned from Sub-global Assessments and other Initiatives. Tech-
Colombia, escala 1:100.000 V1.0. Bogot DC. nical Series No. 58. Secretariat of the Convention on Biological Diversity,
Koschke, L., Frst, C., Frank, S., Makeschin, F., 2012. A multi-criteria approach for Montral.
an integrated land-cover-based assessment of ecosystem services provision to Vanacker, V., Molina, A., Govers, G., Poesen, J., Dercon, G., Deckers, S., 2005. River
support landscape planning. Ecol. Indic. 21, 5466. channel response to short-term human-induced change in landscape connec-
Kroll, F., Mller, F., Haase, D., Fohrer, N., 2012. Ruralurban gradient analysis of tivity in Andean ecosystems. Geomorphology 72, 340353.
ecosystem services supply and demand dynamics. Land Use Policy 29, 521535. Van Hecken, G., Bastiaensen, J., 2010. Payments for ecosystem services: justied or
Lavorel, S., Grigulis, K., 2012. How fundamental plant functional trait relationships not? A political view. Environ. Sci. Policy 13, 785792.
scale-up to trade-offs and synergies in ecosystem services. J. Ecol. 100, 128140. Van Jaarsveld, A.S., Biggs, R., Scholes, R.J., Bohensky, E., Reyers, B., Lynam, T., 2005.
MA, 2005. Ecosystems and Human Well-Being: Synthesis Millennium Ecosystem Measuring conditions and trends in ecosystem services at multiple scales: the
Assessment. Island Press, Washington, DC. Southern African Millennium Ecosystem Assessment (SAfMA) experience. Phil.
Mace, G.M., Norris, K., Fitter, A.H., 2012. Biodiversity and ecosystem services: a Trans. R. Soc. B 360, 425441.
multilayered relationship. Trends Ecol. Evol. 27, 1026. Viglizzo, E.F., Paruelo, J.M., Laterra, P., Jobbagy, E.G., 2012. Ecosystem service evalu-
MADS, 2010. Poltica Nacional para la Gestin Integral del Recurso Hdrico. Ministe- ation to support land-use policy. Agric. Ecosyst. Environ. 154, 7884.
rio de Ambiente y Desarrollo Sostenible, Bogot, DC. Wallace, K.J., 2007. Classication of ecosystem services: problems and solutions.
MADS, 2012. Poltica Nacional para la Gestin Integral de la Biodiversidad y sus Ser- Biol. Conserv. 1, 235246.
vicios Ecosistmicos (PNGIBSE). Ministerio de Ambiente y Desarrollo Sostenible, Wnscher, T., Engel, S., 2012. International payments for biodiversity services:
Bogot, DC. review and evaluation of conservation targeting approaches. Biol. Conserv. 152,
Maes, J., Egoh, B., Willemen, L., Liquete, C., Vihervaara, P., Grizzetti, B., Drakou, E.G., 222230.
Zulian, G., Philipp, J., et al., 2012a. Mapping ecosystem services for policy support Yepes, A., Navarrete, D.A., Phillips, J.F., Duque, A.J., Cabrera, E., Galindo, G., Vargas,
and decision making in the European Union. Ecosyst. Serv. 1, 3139. D., Garca, M., Ordonez, M.F., 2011. Estimacin de las emisiones de dixido de
Maes, J., Paracchini, M.L., Zulian, G., Dunbar, M.B., Alkemade, R., et al., 2012b. Syner- carbono generadas por deforestacin durante el periodo 20052010. Instituto
gies and trade-offs between ecosystem service supply, biodiversity, and habitat de Hidrologa, Meteorologa, y Estudios Ambientales-IDEAM, Bogot, DC.
conservation status in Europe. Biol. Conserv. 155, 112.