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Applied Geography 60 (2015) 1e9

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Applied Geography

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

Do protected areas networks ensure the supply of ecosystem services?Spatial patterns of two nature reserve systems in semi-arid Spain

Antonio J. Castro a, b, *, Berta Martín-L�opez c, Enrique L�opez a, d, Tobias Plieninger c,Domingo Alcaraz-Segura a, e, Caryn C. Vaughn b, Javier Cabello a

a Andalusian Centre for Evaluation and Monitoring Global Change (CAESCG), Biology and Geology Dpt., University of Almeria, 04120, Almería, Spainb Oklahoma Biological Survey, University of Oklahoma, Norman, OK, 73019, USAc Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, 1958, Frederiksberg C, Denmarkd Department of Education, Didactic of the Experimental Sciences, University of Almería, Almería, Spaine Department of Botany, University of Granada, Campus Universitario de Fuentenueva, 18071, Granada, Spain

a r t i c l e i n f o

Article history:Available online

Keywords:BiodiversityEU Biodiversity StrategyFinal ecosystem serviceIntermediate ecosystem serviceNatura 2000 networkRENPA network

* Corresponding author. Oklahoma Biological SurvNorman, Oklahoma, 73019, USA.

E-mail addresses: acastro@ou.edu (A.J. Castro), berL�opez), elopez@ual.es, emlopez@ual.es (E. L�opez),(T. Plieninger), dalcaraz@ugr.es (D. Alcaraz(C.C. Vaughn), jcabello@ual.es (J. Cabello).

http://dx.doi.org/10.1016/j.apgeog.2015.02.0120143-6228/© 2015 Elsevier Ltd. All rights reserved.

a b s t r a c t

Protected areas are essential for conserving biodiversity, and these lands have traditionally been set asidefor this purpose alone. However, the increasing global demand for agricultural and forestry commoditiescreates conflict and tradeoffs between dedicating land for conservation versus food production. Efforts toset aside new lands for biodiversity conservation are compromised by the globally rising demand,creating trade-offs between lands dedicated to conservation versus food production. Ecosystem servicesare the benefits that humans obtain from ecosystems. Recent studies suggest that protected areas pro-vide social and economic benefits that can be used to build political support and raise funds for con-servation. We analyzed the capability of current protected area networks in the semi-arid region of Spainto provide intermediate regulating services (habitat preservation for threatened species, climate regu-lation, erosion control and water flow maintenance) to support the final provisioning service of culti-vated crops to support local communities. We found that existing networks of protected lands supplyconsiderable quantities of ecosystem services, in particular carbon stocks and groundwater recharge. Ourresults demonstrate that the integration of systematic analyses of ecosystem services gaps in protectedarea planning could contribute substantially to safeguarding ecosystem services and biodiversity jointly.However, our study also reveals substantial differences in intermediate ecosystem services supplied bydifferent of protected areas networks, with category VI areas (Natura-2000 sites) generally showing thehighest potential for ecosystem services supply. This demonstrates the important role of Natura-2000sites for preserving regulating services in the European semi-arid region.

© 2015 Elsevier Ltd. All rights reserved.

Introduction

Protected areas constitute a major global effort to preservebiodiversity (Palomo, Martín-L�opez, Alcorlo, & Montes, 2014;Rands et al., 2010). Traditionally, their principal purpose has beento preserve iconic landscapes and seascapes, charismatic speciesand their habitats, and biodiversity hotspots (Haslett et al., 2010;

ey, University of Oklahoma,

ta.martin@uam.es (B. Martín-tobias.plieninger@ign.ku.dk

-Segura), cvaughn@ou.edu

Watson, Dudley, Segan, & Hockings, 2014). Over the past few de-cades, advances in conservation biology and conservation planninghave allowed a precise assessment of the number, extent, andquality of protected areas needed to conserve many viable plantand animal populations (Adams, 2004; Southworth, Nagendra, &Munroe, 2006). Consequently, there is a political goal to integrate17% of the land surface and 10% of the marine surface of the earthinto a global protected area network by 2020 (Secretariat of theConvention on Biological Diversity, 2010). In 2010, the amount ofarea protected globally was 17 million km2 (terrestrial) and 6million km2 (marine), corresponding to 12.7% of the land surfaceand 1.6% of the marine surface (Bertzky et al., 2012). In the Euro-pean Union, around 18% of the landscape is now included in theNATURA 2000 network of protected areas (Bastian, 2013). However,

A.J. Castro et al. / Applied Geography 60 (2015) 1e92

efforts to set aside new lands for biodiversity conservation arecompromised by the globally rising demand for agricultural andforestry commodities, creating trade-offs between lands dedicatedto conservation versus food production (Smith et al., 2010).

The increasing human transformation of the biosphere (Elliset al., 2013) has led to paradigm shifts in how we approach con-servation, moving fromwilderness prioritization towards a ‘peopleand nature’ thinking, in which the dynamics between society andnature are recognized. In this new conservation paradigm, man-agement strategies must consider the tight coupling betweenhumans and nature and include safeguarding human well-being inbiodiversity conservation plans (Kareiva & Marvier, 2012). In thisapproach, protected areas serve to preserve iconic landscapes andspecies as well as safeguard ecosystem services that contribute tohuman well-being (Palomo, Montes, et al., 2014; Watson et al.,2014). Palomo, Montes, et al. (2014) suggest that the manage-ment of protected areas should follow four principles embedded in‘people and nature’ thinking: (i) integration of protected areas intosocial-ecological systems; (ii) establishment of participatory pro-cesses and co-management to reduce social conflicts; (iii) incor-poration of beneficiaries who value, use, or enjoy the ecosystemservices supplied by protected areas in the decision-making pro-cess; and (iv) avoiding location bias of protected areas in mountainsystems through the recognition of their contribution in the crea-tion of multifunctional landscapes able to provide multiple servicesto society.

An ecosystem services approach is essential for implementingthese principles in protected area design and management(Armsworth et al., 2007; Portman, 2013). Ecosystem services,defined as the benefits that humans obtain from ecosystems(Millennium Ecosystem Assessment, 2005), are now widelyviewed as a critical component of conservation strategies (Ng, Xie,& Yu, 2013; Redford & Adams, 2009). There is considerable evi-dence that protected areas provide social and economic benefits tosociety that can be used to build political support and raise fundsfor conservation (Haslett et al., 2010; TEEB, 2012). Consequently,the ecosystem services approach is now being incorporated inglobal protected area and biodiversity conservation policies. Forexample, the International Union for Conservation of Nature(IUCN) World Commission on Protected Areas (WCPA) (Dudley,2008) and the Aichi Targets of the Convention on Biological Di-versity for 2011e2020 have both specified that future protectedarea networks should include ecosystem services (Target 11).Similarly, the Madrid Action Plan for the UNESCO network ofbiosphere reserves established conservation and enhancement ofsite-specific ecosystem services as central goals for biosphere re-serves: “The essence of biosphere reserves as sustainable devel-opment sites could be seen as the effort to design and developplace-specific mixes of supporting, provisioning, regulating andcultural ecosystem services that enable the environmental, eco-nomic and social well-being of resident and stakeholder com-munities” (UNESCO-MAB, 2008).

Integrating ecosystem services in protected areas managementis challenging because traditionally such areas have not beendesigned with the preservation of regulating services (Kremen &Ostfeld, 2005), therefore having consequences in the provision ofother provisioning and cultural services (Laurence et al., 2012;Martín-L�opez, García-Llorente, Palomo, & Montes, 2011; Zorrilla-Miras et al., 2014). Further progress toward management of pro-tected areas for ecosystem services preservation requires advancesin the biophysical quantification and mapping of ecosystem ser-vices supply at landscape scales, including an assessment of syn-ergies and trade-offs between different ecosystem services (Castro,García-Llorente, Martín-L�opez, Palomo, & Iniesta-Arandía, 2013;Castro et al., 2014; Palomo, Martín-L�opez, et al., 2014).

Clearly defining ecosystem services is an important first step intheir valuation. Fisher, Turner, and Morling (2009) suggested thatecosystem services could be classified into intermediate services,final services, and benefits. With this classification, ecosystemprocesses and structure are ecosystem services, but they can beconsidered as intermediate or as final services, depending on theirdegree of connection to humanwelfare. In this sense, intermediateecosystem services can stem from complex interactions betweenecosystem structure and processes (e.g., water recharged by aqui-fers) and lead to final ecosystem services (e.g., crop production),which in combination with other forms of capital provide humanwelfare benefits (e.g., food production).

Here, we analyze the capability of current protected area net-works in the semi-arid region of Spain to provide intermediateregulating services (Fisher et al., 2009). We modeled and mappedthe biophysical provision of intermediate regulating services in twoprotected area networks operating at different organizationalscales in southern Spain to identify spatial gaps. We examined fourintermediate regulating ecosystem services, habitat preservation,climate regulation, erosion control, and water flow maintenance.These services were selected based on their importance for main-taining cultivated crops as a final provisioning service and formaintaining the well-being of local communities (Castro et al.,2014; García-Llorente, Martín-L�opez, Iniesta-Arandia, et al., 2012;García-Llorente, Martín-L�opez, Nunes, Castro, & Montes, 2012;Iniesta-Arandia, García-Llorente, Aguilera, Montes,&Martín-L�opez,2014). We did not include cultural services due to the difficulty inaccurately quantifying their biophysical value (Plieninger, Dijks,Oteros-Rozas, & Bieling, 2013).

Material and methods

Study area

Our study was conducted in eastern Andalusia in the south-eastern Iberian Peninsula and covers approximately 28%(2459 km2) of Almeria province (8774 km2, 700.000 inhabitants,79.7 inhab/km2; Fig. 2). Almeria is semiarid and considered one ofthe driest regions in Europe (Armas, Miranda, Padilla, & Pugnaire,2011), with average rainfall of 250 mm per year (Castro et al.,2011). Winter temperatures vary between 12 and 15 �C, andaverage summer temperatures are as high as 40 �C (L�azaro,Rodrigo, Gutierrez Carretero, Domingo, & Puigdef�abregas, 2001).The area includes all or part of 33 municipalities and localemployment is based on the primary and tertiary sector. The studyarea contains diverse ecosystems including high mountains up to2.611 masl, valleys, coastal zones, saline marshlands, and agricul-tural lands (Fig. 2B) (Castro et al., 2014). We selected this area forseveral reasons. It is a biodiversity hotspot, containing for examplethe Sierra Nevada National Park and Tabernas Desert. It is repre-sentative of the strong need for regulating ecosystem services(e.g., groundwater recharge) for intensive greenhouse horticulture,which has quadrupled the GDP per capita in the last 30 years(National Institute for Statistics, 2005; Wolosin, 2008, 106 pp.).Lastly, it includes protected areas with different levels of Inter-national Union for Conservation of Nature (IUCN) protectionstatus.

Approximately 48% (1154 km2) of the study area is covered byprotected areas in two different protected area networks (Fig. 1):(1) the Andalusian network of protected areas created by theAndalusian Law in February 1989 (RENPA, Spanish acronym for Redde Espacios Naturales Protegidos de Andalucía), which includes27% of the area; and (2) the European Natura-2000 network, whichcovers an additional 21% of the study area. Both protected areasnetworks have as main priorities the conservation of the regional

Fig. 1. Schematic diagram inspired by Mace, Norris, and Fitter (2012) that illustrates the interactions between intermediate regulating services and final provisioning services in thestudy area (Fisher et al., 2009). A includes the ecosystem services in the study in gray boxes, while the indicators used to measure them are indicated by dotted lines. B includes thespatial provision of each ecosystem service based on previous findings by Castro et al. (2014). Red lines represent protected areas boundaries within the area. (For interpretation ofthe references to color in this figure legend, the reader is referred to the web version of this article.)

A.J. Castro et al. / Applied Geography 60 (2015) 1e9 3

natural heritage. The RENPA network consists of 5 protected areas(mean extent: 642 km2), while the Natura-2000 network iscomposed of 3 sites (mean extent: 512 km2). The Natura-2000 siteswere declared as Sites of Community Importance (SCI) in 2006because they harbor priority habitats or species of community in-terest and because they contribute to the coherence of the Natura-2000 network. Hereafter we refer to the Andalusian network ofprotected areas as the RENPA network, and to the additional Sites ofcommunity Importance as Natura-2000 network.

Modeling and mapping the provision of ecosystem services

We modeled and mapped the supply of ecosystems serviceswithin the two protected area networks and the study area as awhole. We used biophysical indicators to assess four intermediateregulating services and a final provisioning service (see Castro et al.,2014 for method details). We identified areas that maintain habitatfor threatened vertebrate species (Fig. 1B-1) with the biodiversitycombined index (BCI model from Rey Benayas and de la Montana

Fig. 2. Map of the study area and protected areas networks. A shows the RENPA network (Spanish acronym for Red de Espacios Naturales Protegidos de Andalucía) and Sites ofCommunity Importance (SCI) of the European Natura-2000 network. B shows the different altitudinal gradients within the area.

A.J. Castro et al. / Applied Geography 60 (2015) 1e94

(2003) and Rey Benayas, de la Monta~na, Belliure, and Eekhout(2006)). We estimated climate regulation from carbon stock mea-surements based on soil organic carbon content (Oyonarte,Almendros, Delgado, P�erez-Pujalte, & Delgado, 1994), density (kg/m3), soil depth horizon (m), lithology types and soil maps (Fig. 1B-2). We used the Universal Soil Loss Equation (USLE model)(Kandziora, Burkhard, &Müller, 2013; Palomo, Montes, et al., 2014)to estimate erosion control as an inverse proxy of soil loss (Fig. 1B-3). We estimated water flow maintenance by quantifying the dis-tribution of potential aquifer recharge expressed as the percentageof the average annual rainfall using the APLIS groundwaterrecharge model (Fig. 1B-4) (Andreo et al., 2008; Quintas-Soriano,Castro, García-Llorente, Cabello, & Castro, 2014). Finally, as a finalprovisioning service (Fig. 1B-5), we quantified crop productionfrom the average annual yields of the most economically importantcrops in the region (tomatoes, cucumbers, zucchini, peppers, andeggplant). A summary of the variables used by spatial models anddata set in ecosystem services modeling and mapping is providedin Table 1 in the Supplementary Data.

We standardized the data to produce a single map of interme-diate regulating services and an additional map of final provision-ing service. We used minimumemaximum normalization tostandardize data on a 0e1 scale following Willemen, Hein, andVerburg (2010). Because this technique is sensitive to minimumand maximum values, and to avoid erroneous transformations dueto outliers, values of ecosystem services maps outside the 5th or95th percentile were assigned the 5th or 95th value respectively(Willemen, Veldkamp, Leemans, Hein, & Verburg, 2012). Interme-diate regulating and final provisioning services were presented andmapped separately using a 1 � 1 km grid.

Assessing the role of protected area networks in safeguardingecosystem services

We compared the overall delivery of intermediate regulatingservices between the two networks (RENPA and European Natura-2000 network) and the non-protected lands. We also exploredwhether there were any significant relationships between thelevel of protection and the amount of each service supplied by an

area. Protection level across both protected areas networkincreased from sites of community importance (IUCN category VI),Natural Park (IUCN category IV), Paraje Natural (IUCN category III),National Park (IUCN category II), and Natural Reserve (IUCNcategory Ia). IUCN category V is not used in the area. Using spatialanalysis techniques (Zonal statistic tool in ArcGIS Spatial Analyst,version 2010) the biophysical provision of each intermediate ser-vice was calculated within each level of protection. We examineddifferences in the provision of each of the intermediate regulatingservices by the different protection levels with the KruskaleWallistest, as the variables were non-normally distributed. Finally, con-servation gaps are defined as non-protected areas that support theprovision of intermediate regulating services and were mapped byidentifying cells/pixels with an equal or higher value of 0.5 inrelation to the final standardized services delivery from 0 to 1(García-Nieto, García-Llorente, Iniesta-Arandia, & Martín-L�opez,2013).

Results

Overall intermediate and final ecosystem service delivery

The biophysical provision of ecosystem services varied acrossthe study area, with the greatest delivery of the final provisioningand regulating services in different regions (Fig. 1B). The biodiver-sity combined index map (BCI in Fig. 1B-1) showed that the wholestudy area is most important for maintaining habitats for birdspecies, followed by mammals, reptiles, and amphibians (see Fig. 1in the Supplementary Data). Soil carbon stocks were largest in thehigh mountains of Sierra Nevada National Park dominated byconiferous and sclerophylous forests (80%) (Figs. 1B-2 and 2B).Erosion control was relatively low throughout the entire study area,with the highest soil losses found in the southern slope of SierraNevada and in the Tabernas Desert (Figs. 1B-3 and 2B), and thehighest groundwater recharge in the G�ador mountain, a karstsystem in the sedimentary mountains (Figs. 1B-4 and 2B). Finally,crop production based on greenhouse horticulture was mainlydelivered in the southern coastal platform of Campo de Dalías(Figs. 1B-4 and 2B).

A.J. Castro et al. / Applied Geography 60 (2015) 1e9 5

Ecosystem services supply by protected area networks

Comparing the resulting maps of aggregated intermediate andfinal services, the overall supply within the RENPA and Natura-2000 network was particularly important for preserving interme-diate services (Fig. 3A). The delivery of the final service mainlyoccurred outside both the RENPA and Natura-2000 networks(Fig. 1B-5).

The overall supply of regulating services differed with pro-tection status within the RENPA network, but also between thesites of community importance (Natura-2000) and non-protected areas (Fig. 4). The mean value of regulating serviceswas highest within the IUCN category VI (Natura-2000 sites) andcategory II (National Park) sites. Category IV (Natural Parks) andcategory III (Paraje Natural) sites showed medium levels ofregulating services supply, which did not differ from non-protected areas. The category Ia (Natural Reserve) site, repre-senting the most restrictive protection status, showed the lowestlevels for regulating services preservation (although it was rela-tively important for habitats for threatened vertebrate conser-vation). Overall, we also observed that all intermediateregulating services were preserved within both protected areanetworks, with the exception of the erosion control in the Nat-ural Reserve since it is actually a marshland (Fig. 4). The pro-tected areas networks, both RENPA and Natura-2000, wereparticularly important for the preservation of carbon stocks andgroundwater recharge and, surprisingly, less important for thehabitat of threatened vertebrates (Fig. 4).

By comparing the spatial mean values for intermediate regu-lating services across the protection gradient (i.e., RENPA network,Nature-2000 network, and non-protected areas), we observed thatoverall the greatest values occurred within the SCI of Natura-2000network, while similar values were observed in RENPA networkand non-protected areas (Fig. 5A). Significant differences in themean supply of all intermediate regulating services were foundacross all levels of protection (Table 1). While mean values ofbiodiversity combined index (BCI) show that the habitat forthreatened species is better preserved in the Natural Reserve, weobserved that National Park and SCI sites of the Natura-2000 weresignificantly relevant for preserving carbon stocks and ground-water resources.

Fig. 3. Spatial patterns of intermediate regulating and final provisioning services provisionservices. B shows the conservation gaps for preserving intermediate regulating services ocsupport the delivery of the set of regulating services. Conservation gaps (in blue) representintermediate regulating services (in the sense of García-Nieto et al., 2013). (For interpretationof this article.)

Conservation gaps in the protected area networks for preservingintermediate regulating services

Our analyses identified several non-protected areas that repre-sent gaps in the preservation of intermediate regulating services(14% of total surface) (Fig. 3B). These gap areas are represented by avalue of intermediate regulating services equal or higher than 0.5(range 0e1). Three priority areas that would be good candidates forincorporating important intermediate services are the northernand eastern portions of the study area (Filabres mountain andTabernas desert in Fig. 2B) for maintaining habitat for threatenedspecies (Fig. 1B-1), and areas on the northern and southern slopesof G�ador mountain for preserving groundwater recharge and car-bon stocks (Fig. 1B-2 and 4).

Discussion

Our findings suggest that current protected area networkssupply only slightly higher levels of regulating services than non-protected areas: only 59% of the total supply of regulating ser-vices occurred within protected areas (Fig. 5B), although theyoccupy 48% of the total surface. Our gap analysis revealed thattargeting the provision of multiple services would require an in-crease of the protected land area surface by an additional 14%.Through such measures, 83% of the total supply of intermediateregulating services would be within protected area networks. Asthis increase in protected area surface in the Spanish semi-aridregion exceeds the international goal of integrating 17% of landsurface in the protected area network, other strategies in conser-vation planning, such as market schemes or payment for ecosystemservices, will likely be required (Chan, Shaw, Cameron, Underwood,& Daily, 2006; Egoh, Reyers, Rouget, Richardson, & van Jaarsveld,2008; Egoh, Reyers, Rouget, Bode, & Richardson, 2009). Our re-sults demonstrate an important spatial trade-off between the cur-rent supply of a final provisioning service (crop production) and theintermediate regulating services needed to support it (e.g.,groundwater recharge). Since the local economy of Almeria prov-ince is mainly supported by agricultural production that directlydepends on groundwater (Downward & Taylor, 2007), our resultssuggest that a payment for ecosystem services (PES) scheme couldhelp resolve this conflict. Farmers could pay for the preservation of

and conservation gaps. A shows the standardized supply of all intermediate regulatingcurred outside protected areas. Conservation gaps describe non-protected areas thatareas with a value an equal or higher than 0.5 from the total standardized delivery ofof the references to color in this figure legend, the reader is referred to the web version

0.0

0.2

0.4

0.6

0.8

Natural Reserve (IUCN Ia)

National Park (IUCN category II)

Paraje Natural (IUCN III)

Natural Park (IUCN IV)

SCI (IUCN VI) Non-protected

Habitat preservation Climate regulation Erosion control Water flow maintenance

Inte

rmed

iate

serv

ices

supp

ly

(spa

tial m

ean)

RENPA NATURA-2000

Fig. 4. Supply of intermediate regulating services expressed as the spatial mean provision across the RENPA network (i.e., Natural Reserve (IUCN category Ia), National Park (IUCNcategory II), Paraje Natural (IUCN category III), and Natural Park (IUCN category IV), and Sites of Community Importance (SCI, IUCN category VI) enlarged by the Natura 2000network, and non-protected areas.

0.0

0.5

1.0

1.5

2.0

Mea

n su

pply

per

pix

el

RENPA network

Natura-2000 network

Non-protected lands

0

20

40

60

80

100 %

of t

oal s

uppl

y in

the

area

RENPA network

Natura-2000 network

Non-protected lands

A) B)

Fig. 5. Overall supply of intermediate services along the protected gradient: RENPA (Spanish acronym for Red de Espacios Naturales Protegidos de Andalucía), Natura 2000 network,and non-protected areas. A shows the spatial mean supply per pixel within RENPA, Natura-2000, and non-protected lands. B shows the percentage of total supply contained alongthe protection level.

Table 1Intermediate and final services supply for all status protection across both the RENPA and Natura 2000 network and the non-protected areas. BCI expresses the BiodiversityCombined Index values used for mapping the habitats for maintaining threatened vertebrates, SCI ¼ sites of community importance. All values are standardized from 0 to 1.

Protection status Protection status Area (km2) Maintaining habitat Carbon stocks Soil loss Groundwaterrecharge

Cultivated crops

IUCNcategory

Protectedarea network

Mean BCI (STD) Dunn Mean (STD) Dunn Mean Dunn Mean Dunn Mean Dunn

Natural Reserve Ia RENPA 529 0.08 (0.09) A 0.05 (0.05) A 0.00 (0.00) A 0.14 (015) A 0 (0.00) ANational Park II RENPA 15,291 0.06 (0.28) B 0.34 (0.34) E 0.11 (0.29) E 0.12 (0.11) C 0 (0.00) AParaje Natural III RENPA 12,816 0.04 (0.23) C 0.14 (0.08) B 0.08 (0.24) CD 0.14 (0.16) C 0 (0.00) ANatural Park IV RENPA 37,351 0.02 (0.31) D 0.18 (0.14) C 0.08 (0.26) D 0.16 (0.26) C 0 (0.00) ASCI VI Natura-2000 51,233 0.02 (0.25) D 0.42 (0.38) D 0.07 (0.23) C 0.52 (0.26) D 0 (0.00) ANon-protected none none 128,627 0.01 (0.26) E 0.19 (0.18) C 0.05 (0.27) B 0.15 (0.24) B 0.2 (0.36) B

KruskaleWallis test 5163.38*** 5884.77*** 6734.44*** 12,507.70*** 4305.80***

The KruskaleWallis test and Dunn groups are used to compare the mean delivery of ecosystem services across the different protection status.*** Statistical significance ¼ 1.

A.J. Castro et al. / Applied Geography 60 (2015) 1e96

those lands necessary for groundwater sources. This approachwould reinforce the idea of including new areas supporting thepreservation of key intermediate services within protectedboundaries.

Although there is consensus that conservation planning andprotected areas can benefit from the ecosystem services approach(Chan et al., 2006; Egoh et al., 2008; Palomo, Martín-L�opez, et al.,2014), it is less clear whether all protected areas successfullycontribute to the preservation of essential ecosystem services. Infact, previous studies have demonstrated that high levels of pro-tection, such as National Park (IUCN category II) and Natural

Reserve (IUCN category Ia), do not ensure the provision of multipleecosystem services (García-Nieto et al., 2013; Palomo, Montes,et al., 2014). However, at the landscape level of the Spanish semi-arid region, our analysis demonstrated that National Parks pro-vide high levels of intermediate regulating services. In contrast, theSCI of the Natura-2000 network with a lower level of restriction, isthe area that provides the highest amount of intermediate regu-lating services. In fact, in more social-cultural terms, stakeholdersfrequently assign higher value to the less restrictive categories ofprotected areas because they perceive a diverse provision ofecosystem services, including provisioning, regulating, and cultural

A.J. Castro et al. / Applied Geography 60 (2015) 1e9 7

services (García-Llorente, Martín-L�opez, Iniesta-Arandia, et al.,2012; Martín-L�opez et al., 2012). Often, it is precisely those pro-tected areas in which local stakeholders are allowed to maintaintraditional management of ecosystems where people are benefit-ting most from the delivery of intermediate regulating services(García-Nieto et al., 2013; Palomo, Martín-L�opez, Potschin, Haines-Young, & Montes, 2013).

This study advances our understanding of the importance ofincluding ecosystem services in land conservation. This studydemonstrates the important role of preserving intermediateregulating services at sites of community importance (IUCNcategory VI). The RENPA network (27% of the surface) preservedonly 23% of intermediate regulating services, while the three extrasites of the Natura-2000 network contributed (with only 21% ofthe surface) as much as 36% of intermediate regulating services.Consequently, although Natura-2000 sites were designed ac-cording to ecological and biogeographical criteria, they also areimportant for preserving multiple ecosystem services (Bastian,2013; Kettunen, Bassi, Gantioler, & ten Brink, 2009). However, todate Natura-2000 networks have rarely been addressed in theecosystem services literature (Kettunen et al., 2009). Our resultsshow the importance of these networks in conserving ground-water recharge and climate regulation, which has been recentlydescribed because of its importance in greenhouse horticulture asthe main driver of the local economy of Almeria province(Quintas-Soriano et al., 2014).

A critical question is whether the food produced by intensiveagriculture in the area and that represents an important final ser-vice for society (Fisher et al., 2009) should be considered anecosystem service. The supply of this provisioning service mainlyoccurred outside both protected area networks, along the coastalplatform of Campo de Dalías. Most of the crops are produced bygreenhouses horticulture, which is extraordinarily dependent onexternal inputs such as synthetic fertilizers, pesticides, plastics,electricity, and fossil fuels. In this study, we considered the foodcoming from greenhouse horticulture as a final provisioning servicesince it provides important benefits to the regional economy. Infact, 86.2% of the total net income of Almería province comes fromgreenhouse horticulture (Sanchez-Pic�on, Aznar-Sanchez, & Garcia-Latorre, 2011), and 5% of the vegetables consumed in Spain comefrom this area (Sanchez-Pic�on et al., 2011). We acknowledge thatthis agricultural production is to some degree decoupled from localecosystems. However, it entirely depends on the availability ofgroundwater resources (Downward & Taylor, 2007), which mostlycomes from aquifers that are recharged in the nearby G�adorMountains (Castro et al., 2014; Quintas-Soriano et al., 2014). Hence,this illustrates how the production of final provisioning services inan area directly depends on the maintenance of intermediateregulating services elsewhere. This is consistent with the frame-work proposed by Haines-Young and Potschin (2010), in whichecosystem services are connected in cascade. The cascade effectfrom specific regulating services (i.e., here groundwater recharge)to provisioning services (i.e., crop production) also highlights theimportant role of protected area networks to ensure the delivery ofmultiple ecosystem services at different spatial scales. However,our study also demonstrates that current protected areas bound-aries do efficiently protect the conservation of threatened verte-brate species, which ultimately was the primary criteria for whichthey were designed.

Finally, our results should be interpreted with some caveats.Although the use of proxies for services quantification is oftenused at large scales, the biophysical proxies used to quantify anecosystems' capacity to supply intermediate services have to beconsidered with limitations. Examples of this include our use ofsoil loss as an inverse proxy for erosion control or the use of soil

carbon stocks as a proxy for climate regulation (Castro et al., 2014).Another example is the estimation of cultivated crops per hectareas a final service. Our assessment would be more accurate if wehad more detailed information on other natural resources (e.g.,water or fertilizers) required to produce zucchini versus eggplant,but these data were not available. Our study is an interdisciplinaryassessment that compares the potential capacity of protectedareas networks to preserve ecosystem services supply at thelandscape level; this approach differs from more traditional,smaller-scale ecological studies. Another important issue is thecriteria used for the design of current protected areas. Both RENPAand Natura-2000 were specifically designed for preserving land-scapes, plant and animal species across unique areas. This is thecase of the National park of Sierra Nevada mountain or the Tab-ernas Desert (Fig. 2B), each considered as global hotspot ofbiodiversity (Blanca, Cueto, Martínez-Lirola, & Molero-Mesa,1998; Mendoza-Fern�andez et al., 2015). This may explain whysome protected areas strongly preserve particular ecosystemservices, such as the case of Natural Reserve for habitat ofthreatened species or forested National Park located for climateregulation.

Conclusions

The Convention on Biological Diversity and other global con-servation policies have expressed a clear need to integrateecosystem services in the design of protected area networks(Haslett et al., 2010). Achieving this goal requires modeling andmapping ecosystem services at the landscape scale. The EUBiodiversity Strategy has an agenda for mapping ecosystem ser-vices to support biodiversity conservation policies (Maes, Egoh,et al., 2012; Maes, Paracchini, et al., 2012). To support the EUBiodiversity Strategy, advanced knowledge about the capacity ofNatura-2000 sites to provide essential ecosystem services such asgroundwater recharge or carbon storage is needed. However, fewstudies have used ecosystem services modeling and mapping forprotected area planning (see Chan et al., 2006; Egoh et al., 2008,2009; Palomo et al., 2013; Palomo, Montes, et al., 2014). Ourassessed five ecosystem services provided by protected area net-works at a regional scale demonstrate that existing networkssupply considerable amounts of ecosystem services, in particularcarbon stocks and groundwater recharge. It further demonstratesthat the integration of systematic analyses of ecosystem servicesgaps in protected area planning could contribute substantially tosafeguarding ecosystem services and biodiversity jointly. How-ever, our study also reveals substantial differences in ecosystemservices supplied by different IUCN classes of protected areas,with category VI areas (Natura-2000 sites) generally showing thehighest potential for ecosystem services supply. This demon-strates the important role of Natura-2000 sites for preservingintermediate regulating services in the European semi-aridregion.

Acknowledgments

Funding for the development of this research was provided bythe Andalusian Center for the assessment of Global Change(CAESCG) (GLOCHARID project), the ERDF (FEDER), Programa deCooperacion Transfroteriza Espanea- Fronteras Exteriores (POXTE-FEX-Transhabitat), Andalusian Regional Government (Junta deAndalucia SEGALERT Project, P09eRNM-5048), and Ministry ofScience and Innovation (Project CGL2010-22314). The OklahomaBiological Survey at the University of Oklahoma at the University ofOklahoma (US) has provided support for A.J.C.

A.J. Castro et al. / Applied Geography 60 (2015) 1e98

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.apgeog.2015.02.012.

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