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Journal of Arid Environments xxx (2017) 1e9

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Journal of Arid Environments

journal homepage: www.elsevier .com/locate/ jar idenv

Ecosystem services provided by biocrusts: From ecosystem functionsto social values

Emilio Rodríguez-Caballero a, b, *, Antonio J. Castro c, d, Sonia Chamizo a, e,Cristina Quintas-Soriano c, d, Marina Garcia-Llorente f, Yolanda Cant�on a, Bettina Weber b

a Departamento de Agronomía, Universidad de Almería, La Ca~nada de San Urbano s/n, Almería, Spainb Max Planck Institute for Chemistry, Multiphase Chemistry, Hahn-Meitner-Weg 1, 55128 Mainz, Germanyc Department of Biological Sciences, Idaho State University, Pocatello, ID, USAd Centro Andaluz para la Evaluaci�on y Seguimiento del Cambio Global (CAESCG), Departamento de Biología Vegetal y Ecología, Universidad de Almería,La Ca~nada de San Urbano, 04120 Almería, Spaine Department of Agrifood Production and Environmental Sciences (DISPAA), Florence University, Firenze, Italyf Sociology of Climate Change and Sustainable Development Research Group, Department of Social Analysis, University Carlos III, 28903 Madrid, Spain

a r t i c l e i n f o

Article history:Received 2 March 2017Received in revised form24 June 2017Accepted 5 September 2017Available online xxx

Keywords:Biological soil crustsDrylandsEcosystem servicesClimate regulationAir quality controlWater regulationErosion control

* Corresponding author. Max Planck InstituteChemistry, Hahn-Meitner-Weg 1, 55128 Mainz, Germ

E-mail addresses: rce959@ual.es (E. Rodríguez-Cacastro@ual.es (A.J. Castro), sonia.chamizodelapiemarina.garcia.llorente@uc3m.es (M. Garcia-Llorente),b.weber@mpic.de (B. Weber).

http://dx.doi.org/10.1016/j.jaridenv.2017.09.0050140-1963/© 2017 Elsevier Ltd. All rights reserved.

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a b s t r a c t

Dryland ecosystems usually show low productivity, considerable water losses and land degradationproblems associated with soil erosion. Most bare-looking areas in these ecosystems are covered bybiocrusts, which represent an important nitrogen and carbon sink and provide essential ecosystemservices. However, until now no studies analyzed the role of biocrusts in providing ecosystem servicesand compared these with the societal perception of biocrust-dominated ecosystems.

In this study, we quantified the direct effect of biocrusts on soil water regulation, erosion control andclimate and air quality in two different semiarid ecosystems dominated by biocrusts, and we exploredthe social importance and perceived vulnerability regarding the capacity of these ecosystems to provideservices to society. Our results disclose an important role of biocrusts in providing four services, withindirect implications on other important ecosystem functions. However, interview partners neitherrecognized the capacity of the two analyzed ecosystems to provide supporting services nor their socialimportance. Survey respondents mostly valued provisioning services related to extraction activities, suchas agriculture, which produce direct economic income but conversely threat biocrust sustainability. Thus,more effort is needed by scientists and policy makers to raise awareness on the key role of drylands withbiocrust communities in preserving ecosystem functions that directly provide regulating services.Moreover, their protection is demanded not only for the provision of key ecosystem services, but alsobecause biocrusts themselves should be considered as communities valued by humans.

© 2017 Elsevier Ltd. All rights reserved.

1. Introduction

Dryland ecosystems represent the largest terrestrial biome ofthe planet and their extension is predicted to increase, reaching upto half of the global land surface by the end of this century (Huanget al., 2016). Vegetation coverage in these regions is limited by high

for Chemistry, Multiphaseany.aballero), castanto@isu.edu,dra@unifi.it (S. Chamizo),ycanton@ual.es (Y. Cant�on),

-Caballero, E., et al., Ecosystem, http://dx.doi.org/10.1016/j.ja

temperature and low, unpredictable, and often torrential rainfall.Mostly dominated by scarce coverage of small shrubs and grasses,drylands are complex socio-ecosystems that host more than 38% ofthe global population (Reynolds et al., 2007). Ecological and socio-economic vulnerability of dryland systems around the world hasincreased during the Anthropocene, as a consequence of humaninduced changes in climate and land use that threatened theirsustainability. These changes demand for policy actions and stra-tegies to ensure dryland conservation while at the same timeprovide human needs (Wilcox et al., 2011). However, dryland ca-pacity to provide ecosystem services is undervalued by society, whohas traditionally perceived conservation as a dichotomy of eco-nomic development and some human well-being components

services provided by biocrusts: From ecosystem functions to socialridenv.2017.09.005

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(Castro et al., 2011; Quintas-Soriano et al., 2016).In dryland systems, apparently bare exposed areas between

vascular vegetation are often covered by biological soil crusts(biocrusts), which are communities that include cyanobacteria,algae, archaea, microfungi, lichen, mosses and other microorgan-isms, growing in intimate association within the uppermost milli-meters of the soil (Weber et al., 2016). As result of theirphysiological activity, biocrusts secrete complex organic com-pounds, like aminoacids, exopolysaccharides and carbohydrates(Rossi and De Philippis, 2015) that contribute to the soil C and Nstock (Elbert et al., 2012), and modify key soil surface propertiessuch as soil texture and porosity (Felde et al., 2014), cohesion andstability and micro-topography (Rodríguez-Caballero et al., 2013).They have been shown to increase infiltration and soil wateravailability (Chamizo et al., 2016), reducing water and wind erosion(Belnap et al., 2014; Chamizo et al., 2016) and nutrient losses(Cant�on et al., 2014; Chamizo et al., 2017), and promoting microbialand vascular plant activity (Dumack et al., 2016; Zhuang et al.,2014). In addition, it has been shown that biocrust-covered sur-faces affect the local and global climate by the modification ofsurface reflectance (Rodríguez-Caballero et al., 2015; Couradeauet al., 2016) and emissivity (Rozenstein and Karnieli, 2015), aswell as a reduction of dust emissions (Belnap et al., 2014) and therelease of climate-relevant reactive N compounds (Weber et al.,2015). All these processes control multiple ecosystem functionsand demonstrate their capacity to supply ecosystem services tosociety, such as climate regulation, air quality control, soil fertil-ization, water regulation, soil protection, and erosion control(García-Llorente et al., 2016). However, the level of public aware-ness on the importance of preserving these communities and theirimportant contributions to society remains poorly studied (Castroet al., 2016; L�opez-Rodríguez et al., 2015).

Biocrusts are particularly sensitive to anthropogenically-relateddisturbances such as land use change and global warming(Concostrina-Zubiri et al., 2014), with natural recovery times thatvary from years to millennia, depending on environmental factors,the magnitude of the disturbance and the time when disturbanceoccurred (Weber et al., 2016). Dry climates, soils of low stability andintense and frequent disturbances result in very long recoverytimes, whereas relatively fast natural biocrust recovery has beenobserved after small disturbances that occurred before the rainyseason on stable soil substrate. However, even when relatively fastrecovery of biocrust coverage occurs, biocrust disturbance directlyaffects their capacity to provide critical regulating services and thefinal soil conditions may differ from the original state. For instance,increased human pressure as a result of maximized social demandsfor provisioning services (e.g. increasing livestock grazing andagricultural production) leads to a decrease of biocrust resistance towater and wind erosion (Concostrina-Zubiri et al., 2016). Thecomplex socio-ecological dynamics between human use andecosystem functioning in drylands produce trade-offs(Concostrina-Zubiri et al., 2016) that cause the general public toperceive the preservation of drylands as a barrier to humandevelopment (Tschakert, 2007). In addition, biocrusts are usuallynot considered as a conservation priority, and thus their integrationin land management and environmental policies remains a chal-lenge from local to global scales.

In the Southeast of the Iberian Peninsula, where drylandsrepresent around half of the territory, similar conditions have beenexperienced. Studies conducted in this region during the pastdecade highlight the crucial roles of biocrusts in soil hydrology,nutrient cycling and functioning of vegetation in these environ-ments (Maestre et al., 2011). However, awareness of their relevanceby land practitioners, the general public or even scientists fromdifferent fields is still limited (Quintas-Soriano et al., 2016). Thus,

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there is an urgent need to explore the level of public awarenessregarding the ecological role of biocrusts. Linking the presence ofbiocrust communities to a series of ecosystem services provided bydrylands will help to increase their visibility and reinforce theirprotection and conservation in threatened ecosystems (Castro et al.,2011; Requena-Mullor et al., 2014).

Over the past two decades, the valuation of ecosystem serviceshas gained importance among scientists and policy-makersworldwide as a way to communicate societal dependence onecological life support systems integrating both natural and socialscience perspectives (Castro et al., 2015). The ecosystem serviceframework is useful for natural resource management (Daily et al.,1997), as it assigns value to nature by translating ecosystem prop-erties into human needs (Harrison, 2010). The variety of ecosystemservices provided by biocrusts can be valued using different ap-proaches ranging from biophysical quantifications to socioculturaland economic approaches. Biophysical quantifications of ecosystemservices such as carbon sequestration or water regulation haverecently been used extensively in conservation applications(Cabello et al., 2012). However, to conserve biocrust functions, weneed to move beyond narrow studies of species or habitat statusand increase the public awareness by emphasizing the variety ofecosystem services delivered to society. To do so, an optimalapproach is to identify an ecosystem's capacity to provide services(supply side) and the social demand for those services (demandside; Martín-L�opez et al., 2014). Addressing both the biophysicalsupply and societal demand of ecosystem services underscores thefact that the importance of an ecosystem service to people isinfluenced not only by the ecosystem's properties but also by so-cieties needs for that service and how that need is perceived.

Here, we first perform an ecological assessment across two siteswith contrasting conservation status to quantify the biophysicalcapacity of biocrusts in preserving a suite of ecosystem servicessuch as water regulation, erosion control, climate regulation and airquality control. We use proxies such as water infiltration, sedimentyield under simulated rainfall, and carbon fixation. Then, byadministering face-to-face surveys of the general public livingnearby or visiting the two sites, we explore the social perception ofthe ecosystem capacity to provide key services to society. Finally,we compare biophysical quantifications with the public percep-tions, discuss potential reasons for the limited perception of therole of biocrusts in dryland functioning, and suggest pathways toincorporate the important role of biocrusts in ecosystem servicemaintenance across Spanish dryland ecosystems.

2. Study areas

2.1. Tabernas badlands

The Tabernas badlands are located in the Tabernas desert,approximately 20 km north of the city of Almeria (N37�0003700,W2�2603000; Fig. 1). Climate is classified as semiarid thermo-Mediterranean with an average temperature of 18.5 �C, a meanannual potential evapotranspiration (ETP) of 1500 mm and anannual precipitation of 235 mm, which indicates a considerableannual water deficit (Rodríguez-Caballero et al., 2014), classifyingthis area as one of the driest ones in Europe. Precipitation isconcentrated in autumn and winter, with a high intra- and inter-annual variability, a relatively high number of rainy days, a highproportion of small rainfall events and a long and continuousdrought in summer (Rodríguez-Caballero et al., 2014). The gulliedlandscape of El Cautivo is dominated by dissected NWeSE valleysformed during a series of geological stabilization and dissectionsequences and presently controlled by climate and surface cover(Alexander et al., 2008). The main soil types are Leptosols, Regosols

m services provided by biocrusts: From ecosystem functions to socialridenv.2017.09.005

Fig. 1. Study area location (a) and overview of the landscape at El Cautivo, Tabernas badlands (b) and Las Amoladeras, Cabo de Gata Natural Park (c).

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and Gypsisols, with a silty loam texture (30% sand, 59% silt and 11%clay; Chamizo et al., 2012a). South and SWorientations show almostno vegetation and shallow soils with little development (EpilepticRegosols). In contrast, North and NE hillslopes have deeper soils(Endoleptic Regosol), mainly covered by biocrusts in the upper andvascular vegetation in the lower part. In some favorable pedimentssoils are thicker and can develop Haplic Calcisols with a dense coverof perennial herbs and dwarf shrubs (Macrochloa tenacissima L.)Kunth (¼Stipa tenacissima L., alpha grass, esparto), Helianthemumalmeriense Pau, Artemisia barrelieri Besser, Salsola genistoides Juss. exPoir., Euzomodendron bourgaeanum Coss, and biocrusts covering thegaps between plants (Cant�on et al., 2003). The most representativetypes of biocrust within the Tabernas badlands are cyanobacteria-dominated and lichen-dominated biocrusts. The first one containsa high cover of cyanobacteria and some pioneer lichens, such asCollema cristatum (L.) F.H. Wigg, Endocarpon pusillum Hedw, Ful-gensia fulgida (Nyl.) Szat, and Fulgensia desertorum (Tomin) Poelt.The lichen-dominated biocrust, which represents a later succes-sional biocrust type, is mainly composed of large squamulose andcrustose lichens, such as Squamarina lentigera (Web.) Poelt, andDiploschistes diacapsis (Ach.), and some cyanobacteria covering thesmall interspaces between lichens.

Water scarcity, low fertility soils and abrupt topography limitland use in the area that is mainly restricted to hunting activitiesand recreational use. Agricultural practices are also performed insome areas to feed game.

2.2. Cabo de Gata Natural Park

Las Amoladeras experimental area is located in Cabo de Gata-

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Nijar Natural Park, close to the Mediterranean Sea (N36�50490100,W2�16W2�150800; Fig. 1). It consists of a semiarid steppe charac-terized by semiarid climate with an average temperature of 18 �Cand mean annual precipitation of 200 mm (Chamizo et al., 2012a).Main soil types are Calcaric Leptosols and Haplic Calcisols (FAO,1998), and soil texture is sandy loam (61% sand, 29% silt and 10%clay). Vegetation is dominated by Stipa tenacissima grasses anddwarf shrubs such as Helianthemum almeriense, Thymus hyemalis,Lygeum spartum, Salsola genistoides, and Launaea lanifera. Biocrustscover around 30% of the interplant spaces and consist mainly ofcyanobacteria- and lichen-dominated biocrusts, with similarcomposition to those from Tabernas badlands, and moss biocrusts.The area is within the Natural Park, which comprises the maximumlevel of protection and a special protection area (SPA). The mainuses in the area include recreational activities, active tourism andmoderate livestock grazing.

3. Material and methods

3.1. Biocrust effects on soil properties and ecosystem processes

3.1.1. Runoff, and erosion measurementsThe effects of biocrusts on runoff generation and erosion control

were analyzed based on previous rainfall simulation experimentson representative undisturbed biocrust communities, referencesoils and biocrust-removed plots within each study site. Infiltrationand sediment yield in the biocrust-covered and biocrust-removedplots were recorded after 1 h of rainfall simulation at an intensityof 55 mm h�1. For a more detailed explanation of the experimentaldesign, see Chamizo et al. (2012a).

services provided by biocrusts: From ecosystem functions to socialridenv.2017.09.005

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3.1.2. Moisture measurementsSoil water content (vol %) was measured at 0e3 cm with EC-5

soil moisture sensors (Decagon Devices, Inc., Pullman, Washing-ton) in undisturbed biocrusts and biocrust-removed soils withinthe two different study areas over a period of one year. Data wereregistered every 10 min and converted to volumetric water content(%) using the Decagon standard calibration equations. Daily soilmoisture was calculated from the 10-min data and then averagedfor each surface type for the whole study period and dry and wetsoil periods (see Chamizo et al., 2016 for more details).

3.1.3. C fixation measurementsTo analyze the effect of biocrusts on atmospheric CO2 removal,

net C flux (balance between CO2 fixation by photosynthesis and CO2emission by respiration) was measured on PVC collars (5 cm heightand 10 cm diameter) containing representative biocrusts and nonbiocrust-covered soils at each site. Nine collars were inserted intobiocrust-covered soils and 4 collars into non biocrust-covered soils.Net CO2 flux was measured using a custom-designed transparentchamber (Ladr�on de Guevara et al., 2015) attached to an infraredgas analyser (LI-6400, Lincoln, NE, USA). The circular chamber wasmade of methacrylate and had a height of 8.5 cm and a diameter of10 cm (in order to fit the collars; volume was 668 cm3). Addition-ally, CO2 efflux was measured in each plot with an IRGA EGM-4 (PPsystems, Hitchin, UK). Five measurements were conducted in eachplot during a day following a rainfall event. Measurements wereconducted under wet soil conditions, when biocrust metabolism isactivated, since they comprise poikilohydric organisms that stay ina dormant state during dry periods (Weber et al., 2016). Data ob-tained during the day were integrated to obtain estimates of daily Cbalances of biocrust and non-biocrust covered soils.

3.2. Social perception of ecosystem services

3.2.1. Social sampling strategyFrom February to April 2012, 228 individual face-to-face surveys

across both sites were conducted. The sampling strategy includedstakeholders residing in or visiting the area. Individuals wererandomly selected from populated areas including parks, restau-rants, recreational areas, and academic institutions. We had nocontact with any of the interviewees in advance of our surveys.Respondents were asked to participate in the study and to respondto a survey related to their perception of the environment in thearea. We informed them that all responses were anonymous, thatwe just wanted to know their opinion, and that there were no rightanswers.

3.2.2. Questionnaire design. Ranking preferences and perceivedtrends of ecosystem services

The questionnaire included questions related to an overallperception of the environment across the two sites regarding thecapacity to provide benefits or contributions to people living orvisiting the area, preferences for ecosystem services as well as theirtrends over the last 10 years. Panels illustrating eight different

Table 1Runoff coefficient (%) and sediment yield (gm�2) after 1 h of rainfall simulation (55mmh�

badlands and Cabo de Gata Natural Park.

Study sity Crust type texture Runoff coefficient (%)

Biocrust Biocrust remove

Tabernas badlands Lichen Silty loam 75 68Dark cyanobacteria Silty loam 58 38

Cabo de Gata Lichen Sandy Loam 39 41Dark cyanobacteria Sandy Loam 63 48

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benefits (or ecosystem services) grouped into provisioning (tradi-tional and intensive agriculture), regulating (climate and waterregulation, air quality, and erosion control), and cultural services(tourism, and local identity) were presented to the interviewees(Supplementary material 1). Respondents were asked if theyperceive that each site provides benefits that contribute to theirwell-being and to the population's well-being (possible answers:very much, much, not very much, and nothing; (Castro et al., 2016)),and examples of potential benefits were requested. All respondentswere asked to indicate the relative importance and perceived trendof each benefit over the past years (e.g., decreased, equal, increased,or don't know) by selecting from the services panel and to name thefour services they consider as most important (supplementarymaterial 1) and to rank them from 1 to 4 (important to essentialservices; Castro et al., 2016). Based on this information, we createdan ordinal measure of the social importance of each service (Castroet al., 2016). Finally, we phrased an open question on what the in-terviewees considered important for the maintenance of ecosystemcapacity to provide different services to society. The answers werelinked to socio-demographic information of the respondents.

4. Results

4.1. Biocrust effects on regulating services

Biocrusts play an important role in providing the four selectedregulating services at both sites: i) soil water regulation throughtheir effect on water infiltration and soil moisture retention, ii)erosion control through sediment loss reduction, and iii) air qualitycontrol and climate regulation through atmospheric CO2 fixation.

As we can see in Table 1, biocrusts showed higher infiltrationthan reference soil in the Tabernas badlands but similar or evenlower infiltration than biocrust-removed soils during rainfallsimulation experiments at both study sites. The combined effect ofbiocrust surface stability and cohesion, on the other hand, stronglyreduced soil erosion in runoff simulation plots when compared tobare soils devoid of them (Table 1). However, the detailed effectsdiffered widely between both study areas. In the Tabernas bad-lands, where soils are characterized by fine texture, low perme-ability and high erodibility, biocrust surfaces reduced the sedimentyield during the rainfall simulation experiment by 80e99%compared to bare surfaces (11e26 g m�2 vs 129e744 g m�2;Table 1). At Cabo de Gata, where the soils are characterized byhigher stability and permeability, the effect of biocrusts was lessremarkable, as they decreased the sediment yield to 13e64 g m�2

during rainfall simulation, representing about 81e83% of thesediment yield on biocrust removed soils.

Biocrusts increased the soil water content in the upper soil layer.At both sites, we observed that the water content was higher in thebiocrust-covered compared to the biocrust-removed soil (Table 2).This effect was particularly strong for the most developed biocrusts(lichen biocrusts), which showed 1.6 and 1.4 times higher watercontent than biocrust-removed soils during wet soil periods inTabernas and Cabo de Gata, respectively.

1), determined for areas with andwithout biocrusts in the two study areas: Tabernas

Sediment yield (g m�2) Reference

d Bare soil Biocrust Biocrust removed Bare soil

76 11 744 648 Chamizo et al., 2012a76 26 129 648e 2 15 e Chamizo et al., 2012ae 15 79 e

m services provided by biocrusts: From ecosystem functions to socialridenv.2017.09.005

Table 2Mean annual soil water content at 0e3 cm, and mean soil water content measured during the wet season (December to April) and dry period (May to August) at sites wherebiocrusts were removed, as well as under cyanobacteria-dominated and lichen-dominated biocrusts at the two study sites: El Cautivo experimental area, Tabernas badlandsand Cabo de Gata Natural Park. Data were registered every 10 min during the hydrological year 2009e2010 and mean values for converted to volumetric water content (%)using the Decagon standard calibration equations.

Soil water content (%)

Tabernas Badlands Cabo de Gata N.P.

Biocrust-removed Cyanobacteria-dominated Lichen Biocrust-removed Cyanobacteria Lichen

Annual 6.4 8.9 9.8 9.5 11.2 13.1Wet soil period (DecembereApril) 12.8 16.3 20.5 18.5 20.3 25.4Dry soil period (MayeAugust) 1.5 2.7 2.2 1.5 2.8 2.7

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After a rain pulse, biocrust photosynthesis and soil and biocrustrespiration were reactivated in the two study areas (Fig. 2). In theTabernas badlands, soil respiration of bare and biocrusted surfacesshowed very similar values (�1.41 ± 0.22 g m�2 day�1 and-1.47 ± 0.42 g m�2 day�1, respectively), which were lower thanbiocrust C fixation by photosynthesis (1.57 ± 0.39 g m�2 day�1),resulting in a slight C gain on biocrusted surfaces (Fig. 2a). At Cabode Gata larger differences in respiration were observed betweenbare soil (�1.13 ± 0.24 g m�2 day�1) and biocrusts (�2.02 ±0.39 g m�2 day�1), and similar to Tabernas badlands, biocrustphotosynthesis was larger than respiration, resulting in a positive Cbalance (Fig. 2b). Thus, whereas after a rainfall pulse, bare areasacted as C sources, biocrusts acted as C sinks.

4.2. Public perception of ecosystem services

Overall, most of the 228 respondents perceived that both studysites have a strong capacity (i.e., very much or much, Fig. 3a) toprovide benefits that are contributing to the population's well-being. In Cabo de Gata Natural Park, more than 80% of re-spondents identified that this area has the capacity to providebenefits (i.e., “very much” or “much”), while less than 5% consid-ered that the area does not provide benefits (i.e., “none”; Fig. 3a). InTabernas badlands, nearly 60% of respondents recognized that thisarea has a strong capacity (i.e., very much) to provide benefits tosociety. On the other hand, it was striking that 33% of respondentsconsidered this area as provider of no substantial benefits (i.e., notvery much), whereas only 6% identified the Tabernas badlands asno provider of benefits (Fig. 3a).

Fig. 2. Carbon fluxes (respiration, photosynthesis and net carbon flux) measured on biocruTabernas badlands; and b) at Las Amoladeras experimental area, Cabo de Gata Natural Park

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Regarding the perceived importance of ecosystem services,most of respondents considered tourism, traditional agricultureand air quality as the most important ones at both sites (Fig. 3b). Incontrast, erosion control, climate regulation and water regulationservices were rarely perceived as relevant. The ecosystem serviceswith the highest and lowest social importance across both siteswere traditional agriculture and erosion control, respectively(Fig. 3b).

The perceived trend (i.e., decrease, stable, increase) ofecosystem services showed differences and similarities betweenboth sites. In both case studies, high numbers of respondentsperceived an increasing relevance for ecosystem services within thefields of tourism and intensive agriculture, while for the relevanceof traditional agriculture the largest decreasewas perceived (Fig. 4).In addition, in the Cabo de Gata Natural Park local identity andwater regulation were perceived with negative trends (Fig. 4a),while services such as climate regulation and air quality wereperceived as having a stable trend. In Tabernas badlands, most re-spondents perceived that the relevance of regulating services(including climate regulation, erosion control, air quality and waterregulation) had declined over the past decade (Fig. 4b), while solelycultural services, recreation and local identity, were perceived witha positive trend.

5. Discussion

Biocrusts modify several soil surface properties and processes(Weber et al., 2016) that provide key regulating services to society(Fig. 5). However, such services are not clearly perceived by the

sted and non-biocrusted surfaces after a rain pulse a) at El Cautivo experimental area,.

services provided by biocrusts: From ecosystem functions to socialridenv.2017.09.005

Fig. 3. Ecosystem service perception at El Cautivo experimental area, Tabernas bad-lands and Las Amoladeras experimental area, Cabo de Gata Natural Park. a) perceivedoverall capacity of each site to provide ecosystem services and b) social importanceperceived for ecosystem services at the two sites.

Fig. 4. Social perception of ecosystem services trend over the last 10 years, a) Cabo deGata Natural Park and b) and Tabernas badlands. The total number of respondents areexpressed as the percentage of all interviewees is shown on the x-axis.

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dryland population that mostly values provisioning services relatedto extraction activities, which are well known to threaten biocrustpreservation. Thus, the proper management and conservation ofdryland regions includes the recognition of the important roles thatthese communities play in the apparently “bare” areas devoid ofvegetation and the increasing political and social awareness of theimportance of nature conservation and biocrust protection.

Our study illustrates that, during intense simulated rainfall ex-periments, biocrusts increased infiltration compared to physicallycrusted bare soils, but showed similar or even lower infiltrationthan soils where biocrust were recently removed (Table 1). Despitethe greater runoff during intense events, higher infiltration rateshave been found on biocrust surfaces during low intensity rainfalls(Rodríguez-Caballero et al., 2013; Chamizo et al., 2016). This higherinfiltration, combined with a decrease in evaporation during wetand cool periods, increased soil moisture when compared withbiocrust-removed soils (Table 2). This effect was particularlyremarkable after rain pulses, when differences between biocrust-covered and biocrust-removed soils were close to 4% of volu-metric soil water content in both study areas (Chamizo et al., 2016).Different effects have been described for other regions where bio-crusts promote runoff generation and increase evaporation(reviewed in Chamizo et al., 2016). Independently of their positive

Please cite this article in press as: Rodríguez-Caballero, E., et al., Ecosystevalues, Journal of Arid Environments (2017), http://dx.doi.org/10.1016/j.ja

or negative effect on runoff generation when compared withphysically crusted bare areas (Chamizo et al., 2016), biocrusts act asrunoff sources for downslope vegetation that efficiently harvestthis runoff and uses it as an extra water supply (Rodríguez-Caballero et al., 2014). As water is the main limiting factor indryland systems around the world (Reynolds et al., 2007), this mayindirectly affect soil nutrient cycling and vegetation primary pro-ductivity. Our results also showed that biocrusts strongly reducedwater erosion (Table 1) within both areas considered in this studyin a similar way as it was shown for many other regions around theworld. At larger scales, the effect of biocrusts on runoff generationand erosion is expected to reduce flow connectivity, modellinglandscape (Rodríguez-Caballero et al., 2014) and avoiding C, N, Pand sediment loss of the ecosystem (Barger et al., 2006; Chamizoet al., 2017). Furthermore, biocrust effects on improved soil stabil-ity and decreased erosion minimize dust production with a strongimpact on climate, freshwater supplies and human well-being(Goudie, 2014). Carbon fixation is also strongly affected by thepresence and development of biocrusts, which showed highphotosynthetic rates after rainfalls (Fig. 2). This effect generallycompensates CO2 emissions by respiration, resulting in a net carbongain that increases soil OC content and fertility when comparedwith bare soil surfaces (Chamizo et al., 2012b). As biocrusts coveraround 30% andmore than 50% of the soil surface at Las Amoladeras

m services provided by biocrusts: From ecosystem functions to socialridenv.2017.09.005

Fig. 5. Ecosystem services cascade framework for biocrust (modified from Haines-Young and Potschin, 2007). The figure describes the linkages between the role of biocrusts insupporting the ecosystem function and the variety of services, benefits and values to society: i) through their effect on key ecosystem processes that provide services to society; ii) asan ecosystem service by themselves; and iii) as an object valued by humans. It also shows how trade-offs between biocrust functioning and anthropogenic pressure lead to areduction of these benefits and how this can be managed by decision makers and politicians.

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and El Cautivo, respectively (Rodríguez-Caballero et al., 2017), theycan be considered as important players in the annual C balance ofboth ecosystems, where vegetation productivity is limited by waterscarcity. Similar results have been observed for different ecosys-tems from hyper-arid to dry sub-humid regions (Gao et al., 2012;Weber et al., 2012). Moreover, it has been demonstrated that bio-crusts play a key role in the N cycle (Delgado-Baquerizo et al., 2013),having direct implications on soil fertility and air quality (Elbertet al., 2012; Weber et al., 2015).

The fundamental role of biocrusts in the different ecosystemfunctions analyzed in this study, and also other well-known effectsattributed to biocrusts, supply important regulating services, suchas water and climate regulation, soil formation and conservation.However, as a consequence of increasing human population, globalwarming and land use change, dryland ecosystems in general, andsemi-arid ecosystems of the Iberian Peninsula in particular, haveexperienced severe degradation (mainly due to land use changedriven by the expansion of intensive agriculture), provoking im-pacts on the supply of ecosystem services (Quintas-Soriano et al.,2016). Concretely, biocrust disturbance as consequence of landuse change such as increased grazing pressure often promotes ashift to degraded, early successional state biocrusts with lowercapacity to provide regulating services to society. In a similar way,also climate change may foster increased soil erosion, as well asreduced C fixation and soil capacity to regulate water availability(Ferrenberg et al., 2015). Based on these results, the need to protectbiocrust communities and include them into conservation plansand land use policies aimed to reduce land degradation is clear.While awareness of biocrust relevance has formed in some areas(e.g. Canyonlands and Arches US National Parks, where biocrustsare recognized as a key and environmentally landscape component

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by tourists), specific efforts devoted to biocrust conservation arescarce or inexistent in most other dryland areas. The imple-mentation of specific conservation practices is probably also limitedby an existing dichotomy between landscape and ecosystemcomponent protection (i.e., biocrusts, in this study) and thedevelopment of provisioning activities (e.g., agriculture andintensive grazing), which are responsible for a drastically reducedbiocrust coverage (Concostrina-Zubiri et al., 2016). In this sense,management policies need to consider the biophysical capacity ofbiocrusts to provide critical ecosystem services and benefits tosociety, but also tradeoffs between extractive provisioning activ-ities and biocrust health, as well as the social implications ofdifferent exploitation land use decisions.

Face-to-face surveys revealed that the local public perceivedboth sites as strong providers of benefits to society. However,although this general perceptionwas solid, we found differences inthe way different services are perceived within the two casestudies. In fact, for the Tabernas badlands, the number of responsesthat considered this site provides “not very much benefits” wassignificantly higher than in the Cabo de Gata Natural Park.This could be interpreted in a way that respondents perceivedthe landscape of Tabernas badlands more negative regardingecosystem service provision. This could be caused by the contrarynature of two sites: Cabo de Gata Natural Park, a popular nature-protected area focused on tourism and coastal activities, versus a“desert area” traditionally known as badlands and with low pro-tection standard and low visitor numbers. Ecosystem services ratedas most important in both sites were tourism and traditionalagriculture (Fig. 3), both associated to economic development andquality of life (Quintas-Soriano et al., 2016). In contrast, as previousstudies have shown, regulating services such as erosion control and

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water regulation were considered as less important (Fig. 3) (Castroet al., 2014). This could be explained by the poor perception thatextreme aridity and arid landscapes are linked to unproductiveecosystems and thus, are undervalued by the general public (Castroet al., 2011). Overall, our results highlight the mismatch betweenthe scientific evidence of the key role of biocrusts as serviceproviding units and the lack of public awareness. This gap is likelycaused by a lack of understanding by local communities of the linksbetween ecosystem services, which are highly valued andperceived by the public (i.e., agriculture), and their role in main-taining the ecological functions which sustain the service cascade(i.e., soil fertility or erosion control) (Fig. 5).

Social perception of the biophysical capacity of ecosystems toprovide services to society is also influenced by land managementstrategies (Quintas-Soriano et al., 2016). At Cabo de Gata NaturalPark, people link a protected area to the maintenance of severalregulating services, such as climate regulation, air quality anderosion control (Castro et al., 2015) (Fig. 4a), whereas in badlandssuch as Tabernas, the high fraction of apparently bare soil causespeople to perceive negative values in ecosystem capacity to providethe same types of services (Fig. 4b). However, in contrast to theseperceptions, current runoff and erosion rates (considering last20 years) are considered as low at the Tabernas badlands site(Rodríguez-Caballero et al., 2014), as a consequence of the lowprecipitation rates but also as a consequence of the strong protec-tive effects of biocrusts (Table 1) and their cross-scale interactionswith vascular vegetation (Rodríguez-Caballero et al., 2014). Theseeffects have indirect implications for economic activities that de-mand for aesthetic values, such as recreation or the film industry(G�amir-Orueta and Manuel-Vald�es, 2007). Furthermore, biocrustscontribute directly to some goods to society. For example, they areconsidered as a model system for biodiversity (Maestre et al., 2016)and several projects around the world highlight the potential ofbiocrust nursery and their artificial inoculation as a biotechnolog-ical tool to recover dryland capacity to provide multiple servicesand goods to society (Xu et al., 2013; Velasco-Ayuso et al., 2016).Both examples should be considered as direct ecosystem servicesprovided to society (Castro et al., 2015).

The lack of perception of the benefits provided by these twoecosystems dominated by biocrusts may in part be influenced bythe poor perception of biocrust existence and their critical role indrylands functioning. It demonstrates the urgency to illustrate theecological roles of these non-charismatic communities and theirrelevance in maintaining key ecosystem functions that provideservices to society (Fig. 5), especially those regulating serviceswhich are perceived in a decreasing trend. Thus, in a similar way asMace et al. (2012) described a relationship between biodiversityand ecosystem services, there are three ways in which biocrustcommunities are linked to ecosystem services: i) as a regulator ofecosystem functions that support dryland capacity to providemultiple ecosystem services (i.e., biocrust effects on soil properties,C, and N fixation that directly affect water cycle, erosion control andsoil conservation); ii) as a final ecosystem service itself (i.e. modelsystem for biodiversity, or restoration community); iii) as a goodthat is subject to valuation (i.e., aesthetic and cultural value ofbiocrust dominated landscapes). Nonetheless, as observed by oursocial assessment, more effort is needed by scientists to translatethe important role of biocrusts in preserving ecosystem functions ofdrylands and the associated goods and benefits to local commu-nities and different actors. In a collaborative process, as e.g., prac-ticed by Science-Policy Interfaces, involved actors, who are aware ofthe impacts of their own everyday actions on ecosystems, need totake responsibility, modify their behavior and transport theirknowledge to the society (L�opez-Rodríguez et al., 2015).

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6. Conclusions

Biocrusts, as a key ecosystem components of semiarid ecosys-tems in south-eastern Spain and many other drylands regionsaround the world, play multiple roles in ecosystem servicesdelivery:

- Biocrusts control several functions that support ecosystem ca-pacity to provide multiple regulating services, such as erosioncontrol, water regulation, and climate and air quality regulation.

- Biocrusts themselves should be considered as an ecosystemservice that directly contribute to some goods.

- Biocrusts as a community have an intrinsic value (aesthetic andcultural) that needs to be valued by humans.

However, our social assessment demonstrates that there is ageneral knowledge gap regarding the services provided bybiocrust-dominated ecosystems and derived benefits to society,which may be caused by missing knowledge on the key role ofbiocrusts in ecosystem functioning. As a consequence, the generalpublic does not perceive biocrust preservation as conservationpriority. We call the need of new environmental education pro-grams that include the diversity of benefits that biocrusts provideto society.

Acknowledgements

This work was supported by the BACARCOS Project (CGL2011-29429) and RESUCI Project (CGL2014-59946-R) founded by theSpanish National Plan for Research. Emilio Rodriguez Caballero andBettina Weber were supported by the Max Planck Society (NobelLaureate Paul Crutzen Fellowship). Antonio Castro is supported bythe NSF Idaho EPSCoR Program and by the National Science Foun-dation under award number IIA-1301792. Special thanks go to theViciana family, owner of El Cautivo, for the permission to use theirland as a scientific experimental site, and to respondents whoanswered our social surveys.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jaridenv.2017.09.005.

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