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Ecology and functional roles of biological soil crusts in semi-aridecosystems of Spain

F.T. Maestre a,*, M.A. Bowker a, Y. Cantón b, A.P. Castillo-Monroy a, J. Cortina c,C. Escolar a, A. Escudero a, R. Lázaro d, I. Martínez a

aÁrea de Biodiversidad y Conservación, Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos,28933 Móstoles, SpainbDepartamento de Edafología y Química Agrícola, Escuela Politécnica Superior, Universidad de Almería, La Cañada de San Urbano S/N, 04120 Almería, SpaincDepartamento de Ecología and IMEM, Universidad de Alicante, Apartado de correos 99, 03080 Alicante, Spaind Estación Experimental de Zonas Áridas, CSIC, Carretera de sacramento, S/N; La Cañada de San Urbano, 04120 Almería, Spain

a r t i c l e i n f o

Article history:Received 31 May 2010Received in revised form6 December 2010Accepted 12 December 2010Available online 7 January 2011

Keywords:Biotic interactionsHydrological processesMediterraneanNutrient cyclingRestorationSemi-arid

a b s t r a c t

Biological soil crusts (BSCs), composed of lichens, cyanobacteria, mosses, liverworts and microorganisms,are key biotic components of arid and semi-arid ecosystems worldwide. Despite they are widespread inSpain, these organisms have been historically understudied in this country. This trend is beginning tochange as a recent wave of research has been identifying BSCs as a model ecological system. Manystudies and research projects carried out in Spain have explored the role of BSCs on water, carbon andnitrogen fluxes, the interactions between BSCs and vascular plants, their dynamics after disturbances,and their response to global change, among other topics. In this article we review the growing body ofresearch on BSCs available from semi-arid areas of Spain, highlighting its importance for increasing ourknowledge on this group of organisms. We also discuss how it is breaking new ground in emergingresearch areas on the ecology of BSCs, and how it can be use to guide management and restorationefforts. Finally, we provide directions for future research on the ecology of BSCs in Spain and abroad.

� 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Biological soil crusts (BSCs), composed of eukaryotic algae, cya-nobacteria, mosses, liverworts, fungi and lichens, cover the upper-most mm of the soil surface in most arid and semi-arid ecosystemsthroughout the globe, and are one of the most conspicuous andimportant biotic components of these areas (Belnap and Lange,2003). They constitute a specialized biotic community that exerta strong influence on key ecosystem processes �including runoffand infiltration (Alexander and Calvo, 1990; Belnap, 2006), soilrespiration (Maestre and Cortina, 2003) and nitrogen fixation andtransformations (Belnap, 2002; Castillo-Monroy et al., 2010)�,influence the establishment and performance of vascular plants(DeFalco et al., 2001; Escudero et al., 2007), and act as habitats fora dependent foodweb of arthropods, fungi, bacteria, and other soilorganisms (Belnap and Lange, 2003).

During the last two decades there has been an unprecedentedupsurge in interest in BSCs worldwide, which has promoted

important advances in our knowledge of the structure, composi-tion, physiology and biogeography of these organisms (see Belnapand Lange, 2003 for a review). Much of this work, however, hasbeen carried out in arid and semi-arid ecosystems of the UnitedStates, Australia, Israel and, particularly in recent years, China.Despite that semi-arid ecosystems comprise more than half of theextent of Spain (Ministerio de Medio Ambiente, Rural y Marino,2008), and BSC communities there were described almost 40years ago (Crespo, 1973; Llimona, 1974; Crespo and Barreno, 1975),their ecology was scarcely studied until the 19900s. This situation isbeing reversed, and nowadays several research groups in Spain areactively studying different aspects of the ecology and biogeographyof BSCs, and their impact on ecosystemprocesses (Fig.1AeF). In thisreview we synthesize the literature on the ecology, biogeography,dynamics and ecosystem impacts of BSCs in semi-arid ecosystemsof Spain. While the focus of this Special Issue is the Spanishsoutheast, we do not restrict this review to this region, as importantstudies have been carried out in areas such as the center of Spain,which hold similar BSC communities (e.g. Maestre et al., 2005;Martínez et al., 2006). With this review we aim to: i) synthesizethe work on BSCs carried out to date in central and SE Spain;

* Corresponding author. Tel.: þ34 914888511; fax: þ34 916647490.E-mail address: [email protected] (F.T. Maestre).

Contents lists available at ScienceDirect

Journal of Arid Environments

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

0140-1963/$ e see front matter � 2010 Elsevier Ltd. All rights reserved.doi:10.1016/j.jaridenv.2010.12.008

Journal of Arid Environments 75 (2011) 1282e1291


ii) illustrate how this research has provided new insights on theecology of these organisms; and iii) discuss future research topicson BSCs, valid for Spain and other regions where these organismsare prevalent. Because of space limitations, this review does notdiscuss in detail all the relevant literature. However, we include inAppendix 1 a compilation of relevant references not explicitlydiscussed in the main text.

2. Composition of Spanish biological soil crusts

Macroscopic components of BSCs are well known in Spain froma floristic, phytosociological and taxonomical point of view (seeAppendix 2 in Supplementary Material for a lichen species

checklist). Among the BSC-forming lichens living in central and SESpain that can be found in bare ground areas located between plantpatches, we can find species such as Aspicilia desertorum, A. fruti-culoso-foliacea, A. hispida, A. fruticulosa, Cetraria steppae, Collemacrispum, C. tenax, Diploschistes muscorum, Endocarpon pusillum,Fulgensia fulgida, F. fulgens, F. subbracteata, Gloeoheppia turgida,Heppia solorinoides, Heteroplacidium imbricatum, Leptogium schra-derii, Peltula patellata, Placidium rufescens, P. squamulosum, Psoradecipiens, P. vallesiaca, Squamarina cartilaginea, S. lentigera, Toniniaalbilabra, T. aromatica, T. diffracta, T. sedifolia, and T. tristis subsp.pseudotabacina. In gypsum soils, which cover large areas of SESpain, we can found some of these species living together withgypsum specialists like Acarospora nodulosa, A. nodulosa var.

Fig. 1. Examples of Spanish semi-arid shrublands (A) and steppes (B), showing the dominance of biological soil crusts (BSCs) in plant interspaces. Close-up views of gypsum andcalcareous BSC communities are shown in C) and D), respectively. Partial views of ongoing climate change (E) and erosion (F) experiments focusing on BSCs. Photo credits: F. T.Maestre (AeE) and Y. Cantón (F).

F.T. Maestre et al. / Journal of Arid Environments 75 (2011) 1282e1291 1283


reagens, A. placodiiformis, Buellia almeriensis, B. zoharyi, Diploschistesdiacapsis, Fulgensia desertorum, F. poeltii, Lecidea circinarioides,L. gypsicola, Lepraria crassissima, Placynthium nigrum, Psora deci-piens, P. savizcii, Teloschistes lacunosus, Toninia coerulea and Xan-thoparmelia pokornyi. The species richness of BSC-forming lichenshas been found to decrease from SE to central Spain (Casares-Porceland Gutiérrez-Carretero, 1993; Maestre et al., 2009b).

The composition of the BSC community changes near higherplants such as Stipa tenacissima L. (Martínez-Sánchez et al., 1994;Maestre et al., 2002, 2009b), which increases nutrient contentand improves microclimate through shade (Martínez-Sánchezet al., 1994; Maestre et al., 2001). In these microsites, the BSCcommunity is enriched both in gypsum and calcareous soils byspecies requiring higher levels of humidity, such as Cetraria acu-leata, Cladonia convoluta, C. subrangiformis or Teloschistes lacunosusand there is a clear increase in the number and cover of bryophytes,mainly mosses, such as Syntrichia ruralis, S. papillosissima, Pleuro-chaete squarrosa, Tortula revolvens, Didymodon acutus and Weissiasp. (Martínez-Sánchez et al., 1994; Maestre et al., 2002; Castillo-Monroy et al., 2010). The same phenomenon has been describedin volcanic soils, where mosses like Acaulon triquetum, Funariapulchella and Phascum curvicolle, and liverworts like Riccia lamel-losa, R. michelli and R. sorocarpa can be found under the canopy ofStipa (Ros and Guerra, 1997).

The taxonomical knowledge of other BSC components, such ascyanobacteria, is not well developed in Spain, as very few studieshave targeted them. The diversity of these organisms can be,however, quite high. Maestre et al. (2006) found more than 15 taxaof cyanobacteria, including Chroococcidiopsis sp. Microcoleussteentrupii, Leptolyngbya boryanum, L. foveolarum, Oscillatoria sp.,and Phormidium sp., associated to BSC-forming lichens from a Stipasteppe in Alicante.

3. Ecophysiology of biological soil crust constituents

All BSC organisms are poikilohydric, meaning that they do notregulate water uptake or loss, but gain it from and lose it to theenvironment passively (Lange, 2003). In dry environments, poiky-lohydric organisms must be desiccation tolerant. When desiccated,all metabolic activity ceases. Thus, water relations and photosyn-thesis are largely coupled, as both photosynthesis and respirationare constrained by degree of hydration and length of hydrationperiods.

In order to maintain biomass and grow, BSC-forming organismshave developed ways of prolonging hydration events or increasingthe number of hydration events. Soil crust cyanobacteria in Spainwere the first microbial organisms observed to move in response tochanges in soil surface drying fronts (García-Pichel and Pringault,2001). These Oscillatoria colonies are composed of filaments ofcells encapsulated in a polysaccharide sheath. Within the sheath,filaments are capable of gliding vertically, “greening” the surfaceupon wetting, then retreating into soil as drying occurred. Theretreat may occur irrespective of light environment, and wasdemonstrated to be an active process requiring energy on the partof the cyanobacteria. This strategy assures that during hydrationperiods exposure to light is optimized, but during desiccationperiods cyanobacteria can wait under the surface where they arebetter protected from other stressors such as UV light.

It has long been known that phycolichens (lichens with green-algal photobionts) are able to become active in the presence ofwater vapour, whereas contact with liquid water is necessary formetabolic activity in cyanolichens (Lange et al., 1986). The Spanishsoil lichen flora is highly dominated by phycolichens. Working inthe Tabernas desert (Almería, SE Spain), Del Prado and Sancho(2007) found that the BSC-forming lichen Teloschistes lacunonus

did not become active under high relative humidity, but activatedreadily when exposed to dew, which may account for up to 12% oftotal rainfall in this region (Moro et al., 2007). The distribution ofthis species seems spatially linked to the commonness of dewdepositions at a regional scale, and total amount of dew depositionat micro-scales. The erect, branching fruticose growth forms seemsparticularly effective in maximizing thallus contact with theatmosphere for dew harvest.

In the absence of regulation of water loss via stomata, ability toretain water is key to extending hydration periods. A study of 14Spanish moss species from xeric, mesic and hydric environmentsrevealed that two prevalent mosses of BSCs, Syntrichia ruralis andPleurochaete squarrosa, had the longest and third longest waterretention times during an experimentally imposed drying event(Deltoro et al., 1998). The authors did not comment upon anunderlying mechanism, thus we can only speculate that this mightbe due to stem or colony morphological characteristics.

Carbon exchange rates vary widely across taxonomic groups ofBSC organisms, and are strongly related to water. In Spain, and ingeneral (Lange, 2003), net photosynthetic rates of lichens are morethan double those of cyanobacterial crusts on an area basis; data onbryophytes are lacking (Table 1). BSC lichens have often beencompared to “sun plants” because their photosynthetic rate tendsto maximize at very high light levels (PPFD�1200 mmol m�2 s�1;Lange, 2003). Further, photosynthetic rates increase as a function oftemperature up to around 25 �C, beyond which they fall again(Lange, 2003). These generalizations would suggest that warm,sunny locations would be ideal habitat, but this is often not thecase. In a comparison of sun and shade populations of the lichenDiploschistes diacapsis at Tabernas, Pintado et al. (2005, 2010) foundthat this species was active only during the 20% of the year, anactivity that mainly occurred during conditions of relatively lowtemperature and PAR radiation. Despite D. diacapsis exhibitedphotosynthetic saturation at high light, and a positive relationbetween photosynthetic rate and temperature, sun populations ofthis species occupied less area, and had less mass per area andthinner photobiont layers. These discrepancies suggest that thisspecies is more likely to occupy shadier habitats and operate undersuboptimal photosynthetic conditions, benefiting from longerhydration times, than to maximize photosynthesis during shorteractivity periods. This would suggest that water availability andhydration times, are the most important in a hierarchy of envi-ronmental controls on field performance.

Sustaining a desiccation event and recovering photosyntheticefficiency upon rehydration is another hallmark of desiccationtolerators. To this end, xeric adapted mosses are able to maintainmaximal levels of quantum efficiency when drying down to about5% water content; in contrast, mosses from wetter environmentsstart experiencing decreases between 20 and 40% water content(Deltoro et al., 1998). They also are much better at maintainingmembrane integrity and avoiding cell leakage, and can regainsimilar levels of quantum efficiency upon rehydration (Deltoroet al., 1998).

4. Biotic interactions in biological soil crust communities

4.1. Interactions between BSC constituents

The study of planteplant interactions in semi-arid areas hascaptivated ecologists since the early days of ecology (e.g., Shreve,1910). Interestingly, and despite the prevalence of BSCs in semi-arid environments worldwide, our understanding of the interac-tions between the organisms forming them is quite limited (seeBelnap and Lange, 2003 for a review). This is particularly true foraspects such as the interplay between facilitative and competitive

F.T. Maestre et al. / Journal of Arid Environments 75 (2011) 1282e12911284


interactions in BSC-forming organisms, which have been virtuallyneglected in the literature despite the renewed interest in this topicamong plant ecologists (see Callaway, 2007 and Brooker et al., 2008for recent reviews).

Although studies on biotic interactions between saxicolous andepiphytic lichens have been carried out since the early 19800s (seeArmstrong and Welch, 2007 for a review), similar studies usingBSC-forming lichens and mosses were not initiated until 20 yearslater (Maestre, 2003a, 2003b; Maestre and Cortina, 2002). Thiswork, carried out in Stipa tenacissima steppes from Alicante (SESpain), studied the patterns of spatial co-variation between BSC-forming mosses and lichens (Cladonia convoluta and Squamarinalentigera), and the effects of Stipa on these patterns. These studiesillustrate the tight relationships between mosses and lichens atdifferent spatial scales, and show the occurrence of significantrelationships between the two lichen species mentioned�particularly close to Stipa tussocks�, suggesting the presence offacilitative interactions between Stipa and C. convoluta.

This work has been recently expanded to study biotic interac-tions among BSC-forming lichens and mosses at the communitylevel using null model analyses of co-occurrence patterns (seeGotelli, 2000 for a review of this methodology). Studies carried outat a single site in central Spain have shown that competition ismore intense than facilitation in BSC communities (Maestre et al.,2008), and that the intensity of competition decreases andincreases whenwater and nutrients are the main limiting resource,respectively (Maestre et al., 2009a). These findings represent thefirst empirical evidence of non-random species co-occurrence inlichen BSC communities. More recently, Bowker et al. (2010a)examined the intensity of biotic interactions at the communitylevel and among species pairs along an environmental stress-gradient spanning about 112,400 km2 over central, S, and SE Spain.These authors observed that negative species interactions wereprevalent in the BSC communities studied, and that competitionintensity increased with the enhancement of abiotic stress (theopposite trend has been predicted for vascular plant communities;Callaway, 2007). They also found that competition was positively

related to species richness at low abiotic stress, and negativelyrelated to richness at high abiotic stress.

Biological soil crust-forming lichens and mosses are funda-mentally different from vascular plants in terms of their facilitativeand competitive mechanisms, and thus the plant-centric mecha-nisms of competition and facilitation �which form the core ofcurrent paradigms (e.g. Tilman, 1988; Grime, 2001; Callaway,2007)� may not apply. Because BSCs are primarily two-dimen-sional, microclimatic buffering and light competition are unlikely tobe key forces structuring them. At high densities, competition foravailable living space between BSC-forming organisms is prevalent.But the absence of facilitation mechanisms common in vascularplants does not imply that facilitation does not occur among BSCconstituents. Lichens and bryophytes exhibit a remarkable array ofsecondary chemicals, some of which have roles in nutrient uptakeand defense against pathogens (e.g., Hauck et al., 2009); thus,species with complementary chemical arsenals may mutuallybenefit by association. Morphological differences may also influ-ence the redistribution of water (discussed below), which couldlead to facilitative species combinations (Spitale, 2009). Finallyparasitism among lichens is common; a lichen mycobiont can stealthe photobiont of other species and overtop the original lichen(Schaper and Ott, 2003); under this scenario, the host is facilitatingthe development of the parasite species.

4.2. Interactions between BSCs and other soil organisms

The only experiment available on this topic from Spain (Castillo-Monroy et al., in press) found that the presence or absence ofspecies in the bacterial community of a gypsum steppe located inCentral Spain (Belmonte de Tajo, Madrid) was insensitive to the BSCcommunity structure; however, therewere several sensitive bacterialspecies. Some lichens, including Fulgensia subbracteata and Toniniaspp., exhibited apparent antibacterial activity, while Diploschistesdiacapsis consistently affected sensitive bacterial species, sometimespositively. These results high light the role of the composition andstructure of BSC in modulating their effects on microbial

Table 1A summary of measurements relevant to biological soil crust photosynthesis from Spanish studies. See the original articles for details on the experimental treatments/populations studied in each case.

Study Material Treatments Chl a(mg m�2)

Chl aþ b(mg m�2)

Net CO2 exchange(mmol m�2 s�1)

Quantumefficiency PSII

Maestre et al. (2006) Synthetic cyanobacterialand lichen crusts

Fragment inoculation, without fertilization,watering

27 37 1.9a

Fragment inoculation, without fertilization,no watering

19 30 0.6a

Fragment inoculation, fertilization,watering

70 81 2.2a

Fragment inoculation, fertilization,no watering

45 58 0.8a

Slurry inoculation, without fertilization,watering

45 55 2.5a

Slurry inoculation, without fertilization,no watering

33 45 1.7a

Slurry inoculation, fertilization,watering

69 80 3.2a

Slurry inoculation, fertilization,no watering

42 47 2.3a

Pintado et al. (2005) Diploschistes diacapsis Sun population 1350 5b 0.28c

Shade population 1780 4.13b 0.25c

Del Prado andSancho (2007)

Teleoschistes lacunosus Two habitat types 0.6e0.7

Deltoro et al. (1998) Pleurochaete squarrosa andSyntrichia rurales,field conditions

P. squarrosa 0.53e0.56S. ruralis 0.53e0.57

a ¼ values reflect treatment means.b ¼ values reflect maximal rates, andc ¼ coarse estimate converted from quantum yield.



communities.Given thatmost studiesonthis topichaveevaluated theeffects of broad types of BSC (e.g. crust dominated by lichens andmosses vs. crust dominated by cyanobacteria) on particular groups ofmicroorganisms (e.g., Yeager et al., 2004; Soule et al., 2009), futurestudies should explicitly consider BSC attributes such as diversity andcompositionwhen evaluating BSC-microbial interactions.

4.3. Interactions between BSCs and vascular plants

It is well known that BSCs exert a strong influence on theestablishment and performance of vascular plants (Belnap andLange, 2003). Empirical evidences of the effects of BSC on theseplants are numerous but contradictory, ranging from negative topositive (e.g., Anderson et al., 1982; DeFalco et al., 2001; Hawkesand Menges, 2003). However most of these studies have consid-ered both the plant and BSC communities as a whole, withouttaking into consideration the species involved. As part of a morerecent effort to unveil the relation between both plant and BSCdiversity in these ecosystems, a small set of works have exploredspecies-specific responses of vascular plants to BSCs (e.g., Zaadyet al., 1997; Hawkes and Menges, 2003), sometimes consideringsome broad structural BSC classifications (Rivera-Aguilar et al.,2005). These studies have also found contradictory BSC effects onvascular plants but corroborated the importance of BSCs as a keymodulator of seedling emergence and performance.

This controversy is probably a consequence of the fact thatplanteBSC interactions are likely to be highly species-specific,similarly to the situation found with planteplant interactions(Callaway, 2007). If so, diverse responses are expected dependingon the composition and structure of both BSC and plant commu-nities. To test this hypothesis, Escudero et al. (2007) experimentallyevaluated the effect of two dominant lichens (Squamarina lentigeraand Diploschistes diacapsis) on the emergence of three gypsophytesfrom central Spain. They found significant and different effects ofSquamarina lentigera and Diploschistes diacapsis on the three plantspecies studied. In addition, Escudero and Martínez (unpublisheddata) have evaluated the effect of BSC-forming lichens on theemergence of annual gypsophytes during a six-year period on wellconserved gypsum outcrops from central Spain. They found thatthe relationships between BSC and vascular plant species wereextremely complex, with repulsions, attractions and neutralresponses between components of both communities at the specieslevel. The potential mechanisms underlying these interactions arealso complex, and involve plant traits related to seed morphologyand dispersal, and BSC traits such as the existence of allelochem-icals and the morphology of the thallus (foliose or crustose), whichare highly related to their function (Bowker et al., 2010b). Theseresults illustrate the importance of species-specific interactionsbetween vascular plants and BSC-forming soil lichens to under-stand how BSCs affect plant composition and structure.

Most studies on the interaction between BSCs and vascularplants have focused on seed germination and early phases ofseedling establishment. Conversely, the effects of BSCs on adultplants have scarcely been studied. In a recent work, Cortina et al.(2010) found that BSC disturbance had a weak effect on short-term performance of neighbor Stipa tenacissima tussocks in a semi-arid steppe from Alicante. Yet, killing the BSC with herbicide hada significant effect on the water use efficiency of this species.

5. Role of biological soil crusts on ecosystem functioning

5.1. Effects on nutrient cycling

Semi-arid ecosystems of Spain are characterized by a sparsevegetation cover, which is often arranged as a two-phase mosaic of

vegetated and bare ground patches (Puigdefábregas et al., 1999;Maestre and Cortina, 2002). Distribution of soil nutrients in theseareas is strongly linked to discrete plant patches, and the formationof “resource islands” has been reported under the canopy of widelydistributed plant species, such as Stipa tenacissima and Retamasphaerocarpa (L.) Boiss. (Maestre et al., 2001; Pugnaire et al., 2004;Goberna et al., 2007). However, a large proportion of the soil inthese ecosystems is unvegetated and covered by BSCs. Therefore,most nutrient inputs to and losses from semi-arid soils must passthrough the soil boundary created by these organisms (Belnapet al., 2003). Indeed, the role of BSCs as a key modulator of thecarbon (C) and nitrogen (N) cycles has long been acknowledged(e.g. Calder, 1959), and has been thoroughly studied during the lastdecades (see Belnap and Lange, 2003 for a review).

Recent research is showing the important roles BSCs have inmodulating C and N heterogeneity and cycling in semi-aridecosystems from Spain. Castillo-Monroy et al. (2010) found that,over a two year period, in situ availability of NH4

þ-N under plantcanopies (Stipa and Retama) did not differ from that found underadjacent bare soil and BSC-dominated microsites in a semi-aridsteppe located inAranjuez (central Spain).However, the rateofNO3

�-Nproduced in thefield, aswell as the potential nitrification rate,wasreduced under BSC-dominated areas compared to bare groundmicrosites andsoils locatedunderplant canopies (Fig. 2). In the samestudy area and period, Delgado-Baquerizo et al. (2010) reported

Stipa Retama Bare soil Low Medium High

NH

4 - N

(µg

cm-2

day-1

)µg

cm

-2da

y-1)

0.02

0.04

0.06

0.08

0.10

NO

3 - N

(

0.2

0.4

0.6

0.8

1.0

1.22007 2008

BSC cover

Fig. 2. Annual changes in NO3�-N (upper graph) and NH4

þ-N (lower graph) availabilitybetween five microsites in a semi-arid Stipa tenacissima steppe from central Spain.Stipa ¼ Stipa tenacissima tussocks; Retama ¼ Retama sphaerocarpa shrubs; Bare soil,Low, Medium and High indicate areas with very low (<5% cover), low (5e25% cover)medium (25e75%) and high (>75%) biological soil crust (BSC) cover. Note the differ-ences in scale in the y-axis. Data represent means � SE (n ¼ 4 surveys). Data adaptedfrom Castillo-Monroy et al. (2010).



mean N availability values ranging between 51.2 mg N kg�1 soil and25.5mg N kg�1 soil (0e4 cm depth) for areas with high and low BSCcover, respectively. NO3

�-N was the dominant N form for bare soilmicrosites and low BSC cover areas, but dissolved organic Nwas thedominant N form when the BSC cover was high. By using experi-mentalmanipulations (surface soil cutting and herbiciding), Cortinaet al. (2010) evaluated the effect of the physical structure and thebiotic component of BSCs on soil N dynamics in a semi-arid steppefromAlicante. Herbicide applicationhad a strongeffect onNfixationactivity, suggesting that the populations of N-fixing cyanobacteriaand cyanolichens may have been reduced for an extended period oftime. In contrast to herbicide application, physical alteration of thesurface soil did not affect BSC ability to fix atmospheric nitrogen.Maestre et al. (2006) evaluated the functioning of BSC-inoculatedsoils in a microcosm experiment, and found that this inoculationsignificantly increased the C and N fixation of the soil. Maestre andCortina (2003) found a high degree of spatial variability in soil CO2flux in a semi-arid steppe from Alicante, largely attributable to cor-responding heterogeneity in cyanobacteria and lichen-dominatedBSCs. In this study, BSC-dominated microsites had significantlyhigher soil respiration during spring than bare ground areas. Similarresponses have been observed after three years of in situ measure-ments in a gypsum Stipa tenacissima steppe located inAranjuez (A. P.Castillo-Monroy & F. T. Maestre, unpublished data). At this site, andwhencompared tobaregroundareas, soil respiration increasedwithincreases in BSC cover. In the same direction, Maestre et al. (2005)also found a positive relationship between the total cover of BSCsand soil respiration (measured in the laboratory under optimaltemperature and moisture conditions) in BSC-dominated ecosys-tems from Madrid and Alicante. However, ongoing research beingcarriedout in twocalcareous Stipa steppes fromAlmería (SESpain) isshowing that, over a three-year period, soil respiration in BSC-dominated areas does not differ fromthat foundunder the canopyofStipa and bare ground areas (A. Rey, unpublished data). Futurestudies need to be done to explain these differences, which may bedue to soil and climatic differences between study areas, and to fullyunderstand under which conditions BSCs modulate soil respiration.

Other studies have attempted to partition the effects of particularattributes of BSC communities (cover, diversity and biotic interac-tions) on nutrient cycling indicators. At small spatial scales (a singlesite located in Belmonte de Tajo), attributes such as BSC cover andspecies richness explained a substantial part of the variation foundin variables such as the activities of the b-glucosidase and ureaseenzymes (Bowker et al., 2010b). Increases in cover and richnesspromoted an increase on the activity of these enzymes, and thus onnutrient cycling. At this site, very little of the effects of BSC attributeson ecosystem function could be ascribed to changes within thebacterial community, suggesting a primary importance of thelichens themselves (Castillo-Monroy et al., in press). Maestre et al.(2005) found that the richness and evenness of BSC communitiesnegatively influenced the amount of total soil N in two semi-aridecosystems from Madrid and Alicante, suggesting that N inputs inthe soil were related to the abundance of particular species. Atregional spatial scales (a 112,400 km2 area encompassing central, S,and SE Spain), climatic variables were the main driver of changes inthe activities of the b-glucosidase and phosphatase enzymes(Maestre et al., 2010). Of secondary importance were the effects ofcommunity properties such as total cover, which in the case ofphosphataseweremoderately strong. At this spatial scale, increasesin BSC cover led to increases in the activities of these enzymes.Species interactions also indirectly affected ecosystem functioningvia their moderate effects on community properties such as cover.

These regulatory roles of BSCs in nutrient cycling are very likelysubject to change under shifting climate regimes. Ongoing experi-mental manipulations of temperature and rainfall are also being

carried out at Aranjuez (Fig. 1E). In this area, we are evaluating soilCO2 flux and N responses to simulated climate change in plots withand without BSCs to explore the role of BSC communities asmodulators of ecosystem responses to ongoing climate change.Preliminary results from the first year of this experiment show thataverage increases in temperature of 2.6 �C year�1 promote a slight,but not significant, increase in soil CO2 flux in the plots without BSC(Maestre et al., 2010). However, such an increase was clearlysignificant in plots with well developed BSCs. The amount of CO2respiredover the studyperiodperunitof BSC coverwashigher in theelevated temperature plots. These results provide evidence of strongshort-term effects of the increase of temperature on soil respiration,a response that was controlled by total BSC cover (i.e. areas of lowBSC cover didnot showany response to thewarming treatment), butnot by BSC richness, evenness or biotic interactions among BSCconstituents. They also indicate that, if warming increases soilrespiration particularly in areas of high BSC cover, BSC-formingorganisms such as lichens and mosses may be at risk of C deficits ifthey do not increase their photosynthetic rate concomitantly.

5.2. Effects on water fluxes and erosion

In the arid and semi-arid ecosystems of SE Spain, BSCs havea large impact on infiltration and erosion processes. Several workshave analyzed the influence of BSCs on runoff and erosion at smallspatial scales in badlands systems, mostly developed on marls,under simulated (Alexander and Calvo, 1990; Calvo-Cases et al.,1991; Solé-Benet et al., 1997; Chamizo et al., 2009) and natural(Cantón et al., 2001) rainfall events (Fig. 1F). These studies reporteda wide variation of runoff coefficients on BSC-dominated surfaces,ranging between 11 and 72% under extreme simulated rainfalls (1 hduration; 50e55 mm h�1 constant rainfall intensity and dry condi-tions), and between 0 and 71% for natural rains (Fig. 3). Erosion ratesalso vary substantially, both under natural rainfalls and simulatedrain, with values between 5 and 150 g m�2 after extreme simulatedrainfall events (Calvo-Cases et al.,1991). This variability is attributedto the interaction of factors like the characteristics of the underlyingmaterial (Calvo-Cases et al., 1991; Chamizo et al., 2009), the slopegradient (Solé-Benet et al., 1997; Chamizo et al., 2009) and thefunctional traits of the species forming the BSCs. The composition ofthe BSC community has been identified as a key factor to explain thedifferences in erosion. For example Chamizo et al. (2009), under thesame environmental conditions, found reduced runoff coefficientson mosses (about 12%), while for crustose and squamulose lichensthese coefficientswerehigher than60%. Furthermore, BSCs areoftenassociated with varying degrees of physical crusting and the varia-tion in the proportions of physical crusts and different types of BSCsaffects runoff and sediment yield. Other properties of BSCs, such asroughness (Chamizo et al., 2009), porosity (Alexander and Calvo,1990) and hydrophobicity (Souza-Egipsy et al., 2002) have beenidentified as key factors controlling the variability in runoffresponse. Twocommonpatterns are highlighted from these studies:infiltration is lower in BSCs than in plant covered patches and inmany cases comparable to physically crusted soil (Fig. 3), and thepresence of BSCs significantly reduce sediment yield at the patchscale (Calvo-Cases et al., 1991; Solé-Benet et al., 1997; Cantón et al.,2001). Nevertheless, the effect of that additional runoff from BSCspatches on erosion has to be evaluated at larger spatial scales,especially in ecosystems where BSCs cover complete landforms,because it can increase erosion risks downslope or favors waterharvesting in vegetated areas.

In semi-arid Stipa tenacissima steppes from SE Spain, watertypically flows from the bare ground areas to the vegetated patches(Cerdá, 1997; Maestre et al., 2002), enhancing their productivity(Puigdefábregas et al., 1999). Maestre et al. (2002) found that



differences in the composition of the BSC community contributedto the increased infiltration found under the canopy of tussocks, ascyanobacteria�that dominated the BSC community in bare groundareas� were negatively related with infiltration. Eldridge et al.(2010) evaluated the effects of Stipa, BSCs and rabbits (Oryctola-gus cunniculus) on infiltration processes in Aranjuez. They foundthat at the landscape scale, both Stipa tussocks and BSCs promotedinfiltration, whereas rabbits compromised the crust effect. Thiseffect of BSC was initially unexpected, but was explainable by therelative prevalence of mosses, mostly infiltration promoters, versuslichens, runoff promoters. This study illustrates, for the first time,the relationships between crust species level community structureand ecosystem function in the form of infiltration, and demon-strates one reason why BSCs behave differently at locations withdifferent suites of components.

Very little is known about the influence of BSCs on othercomponents of the water balance. Over a 43-month monitoringperiod, A. P. Castillo-Monroy& F. T.Maestre (unpublished data) havefound important variations in soil moisture between bare soil andareas with medium (25e75%) and high (>75%) BSC cover ina gypsum area from central Spain (Appendix 3). These authorsobserved higher moisture under medium BSC cover, particularlyafter spring and autumn rainfalls. These resultsmaybe promoted bythe reductions in infiltration promoted under high BSC covermicrosites, as many of these microsites are dominated by lichens

such as Diploschistes diacapsis, which can seal the soil surface. In theTabernas desert, Cantón et al. (2004) showed that soil lichens canpreserve soil water in summer, an effect attributed to the reductionof evaporation promoted by the structure of lichens, which iseffective in retaining water at the lichenesoil interface (Souza-Egipsy et al., 2004), and to the white color of some lichens (e.g.Squamarina lentigera, Lepraria crassissima and Buellia zoharii), whichfavors the reflectance of solar radiation and lowers temperatures.Lázaro et al. (2008) showedhowdifferent BSC communities living atTabernas had contrasted microclimatic features. They found thatPAR radiation and surface temperature were considerably lower inall the lichen-dominated communities than in cyanobacteria-dominated communities, whereas soil moisture and the duration ofdew deposition (minutes during which lichen temperature wasunder the dew point temperature) were higher in the formercommunities. These results suggest that differences in BSC compo-sition affect both evaporation and dew deposition.

6. Dynamics of biological soil crusts after disturbances

Ongoing studies being carried out at Tabernas are providingimportant insights regarding the colonization capacity and growthof different BSC species and communities after disturbances. Inareas where BSCs have been removed, the dominant species of thesurrounding BSC community are often the best colonizers (Lázaroet al., 2008). However, cyanobacteria and some lichen species,such as Placynthium nigrum, Squamarina lentigera and Fulgensia sp.have been found to be good colonizers in all sites. Early-succes-sional BSC communities (dominated by cyanobacteria, fungi andalgae) showed the largest recovery capacity at Tabernas (28.3% inaverage 1 year after experimental BSC removal), followed by thosedominated by Diploschistes diacapsis (21.1%) and S. lentigera (14.6%);communities dominated by Lepraria crasissima had the smallercapacity of recovery after disturbances (4.7%; R. Lázaro, unpub-lished data). Different results have been reported from centralEurope, where the removal of BSCs promoted the replacement ofcyanobacteria/algae by macro-cryptogams like lichens and mosses(Langhans et al., 2010). These authors did not find significantdifferences between BSC removal treatments and controls after twoyears from treatment application, showing that succession andrecovery processes depend on rainfall patterns, and are differentand much faster in central Europe than in SE Spain.

Belnap and Eldridge (2003) provided data about recovery timesranging from decades to centuries (depending on crust type, soiltype, severity of disturbance, and climate) from semi-arid NorthAmerica and Australia. However, they stated that recovery time ismuch faster in soils with inherent aggregate stability, which arecommon in SE Spain (e.g. Rillig et al., 2003). Indeed, results fromTabernas show yearly increments in total BSC cover after distur-bances as large as 30%, and decadal recovery times after BSC removalare expected in this areaunder lowerosion levels (Lázaroetal., 2008).In this site, disturbed areas thatwere completely void of BSCs in 1990showa90%of cover of these organisms today (R. Lázaro, unpublisheddata). However, recovery rate at Tabernas has been found to be quitevariable, and depends not only of BSC type but also on the microcli-matic oscillations andon rainfall erosivity (Lázaro et al., 2008). Underlowerosion conditions,maximum individual growth ratesmeasuredat this site after experimental BSC removal varied between 0.5 and1.5 cm2 year�1, depending on the species considered and on overallclimatic conditions (R. Lazaro, unpublished data).

Bevan (2009) studied the resistance of several dominant BSC-forming lichen species to drop impacts and their sensitivity totrampling at Tabernas. She found unexpected small inter-specificdifferences in such resistance, which was much larger than thatfound in soil aggregates immediately under the same crusts. This

VP BSC-HC BSC-LC PC

Eros

ion

rate

s (k

g·m

-2)

0.0

0.2

0.4

0.6

0.8

1.0

1.2

Run

off c

oeffi

cien

t (%

)

0

20

40

60

80 Mean Maximum

Fig. 3. Mean annual runoff coefficient (ratio between runoff rate and rainfall) anderosion rates, and maximum runoff coefficient and erosion rates registered in a singlerainfall event in different microsites during three hydrological years in the TabernasDesert (Almería, SE Spain). Data were recorded after natural rainfalls in circular micro-plots (0.24 m2) with different types of soil cover. Micro-plots with biological soil crusts(BSCs) consist in a mix of lichens and cyanobacteria. VP ¼ vascular plants, BSC-HC ¼ high cover (>90%) of BSCs, BSC-LC ¼ low cover (<50%) of BSCs, and PC ¼ physicalsoil crust. Error bars indicate SD (n ¼ 3).



explains the strong positive effects of BSCs in protecting the soilagainst erosion and suggests positive feedback processes in BSCdevelopment, at least from a certain BSC cover threshold (Lázaroet al., 2008). In spite of their resistance to erosion, BSCs from Tab-ernas were mechanically fragile (as found in many other areas;Warren and Eldridge, 2003), especially when they were dry, beingthe BSC dominated by cyanobacteria more resistant to tramplingthan that dominated by lichens.

7. Restoration of biological soil crusts

Given the key roles they play in maintaining ecosystem structureand functioning, restorationofBSCs shouldbeundertakenwhen theycan contribute toward reestablishment of a more highly functionalecosystem. In general, restoration practitioners have barely consid-ered BSCs in theirwork (Bowker, 2007). This is particularly true in SESpain, as most restoration efforts carried out there have prioritizedthe increase in forest cover (Maestre and Cortina, 2004a). The lack ofattention to BSC in restoration practices is not surprising, as aware-ness on the role of BSCs and their effects on ecosystem services isminimal, and most information available on the functional role ofBSCs in the region comes from small scale experiments, whoserelevance at the scale of management is unknown.

As illustrated in the preceding section, the rate of spontaneousBSC colonization of degraded areas, once the stress factor isreleased, may be faster than initially expected. Albeit the dataavailable do not allow the establishment of generalizations,observations from SE Spain suggest that this rate is fast enough tostart considering these organisms during restoration activities.There are two primary situations where BSCs may have a role toplay in restoration in SE Spain: degraded Stipa tenacissima steppes,and roadside or quarry revegetation. Wooded Stipa steppes wereprobably impoverished for centuries by fuel wood harvesting andcropping of this grass (Cortina et al., 2009; Maestre et al., 2009b).Most Stipa steppes in SE Spain are currently at this somewhatdegraded ecosystem state (Maestre and Cortina, 2004b). Furtherpressure leads to a state of reduced plant cover and local scaleerosion. We clearly need research to determine if BSCs wouldimprove ecosystem recovery at this stage. As discussed above, BSCcolonization might increase soil stability and protect the soilagainst drop impacts, generate runoff that may be recaptured byimpoverished Stipa cover, and increase C and N contents comparedto bare soil, as found in steppes from central Spain (Castillo-Monroyet al., 2010). One the other hand if BSCs are partially composed ofmosses, infiltration may be enhanced, as has been recentlydemonstrated in a Stipa steppe from central Spain (Eldridge et al.,2010). The restoration of roadsides and quarries may benefit fromassisted recovery of BSCs, as promoting these organisms in theseareas would help stabilize the soil surface, fix atmosphericnitrogen, and potentially create the heterogeneity needed toincrease plant production in vegetated patches.

Restoration techniques explicitly based on BSCs have not yetbeen tested in Spain, but some research has addressed nutrient andwater constraints that may limit BSC recovery under field condi-tions. Maestre et al. (2006) studied cyanobacterial colonization ofbare unfertile soil by applying either BSC fragments or slurry, withand without organic amendments, and maintaining the soil ina growth chamber. Surface soils were watered twice and 5-timesaweek to80%field capacity. Sixmonths after inoculation, they foundthat cyanobacteria density was high enough to show a distinctiverate of C and N fixation, and aggregate the 2 mm surface soil.Watering frequency increased cyanobacterial activity by as much as8 times, and organic amendments were also effective.

Thus we know that in combinationwith inoculation, eliminationof moisture and nutrient constraints may result in rapid

cyanobacteria establishment, although field trials are lacking.Provision of inoculationmaterials are the limiting factor at this time.Inoculation may be carried out by transplanting field-collected BSCmaterials (Maestre et al., 2006;Bowker, 2007). This techniquehas theadvantage of using local organisms, but it is destructive andmayonlybeapplicable at small scales. In contrast, applicationof commercially-available inoculums, produced ex-situ, ensures a homogeneous,controlled and accessible source of cyanobacteria, and can be easilyapplied using standard hydroseeding systems. Disadvantages of thistechnique are the current lack of locally available products, and thelack of inoculum produced with local genotypes.

8. Conservation of biological soil crusts

A Spanish Red List of endangered BSC-forming organisms iscurrently lacking. However, some regional Red Lists have beendeveloped in order to detect those lichen species with currentconservation problems. Atienza and Segarra (2000) publisheda preliminary Red List of the lichens of the Valencian Community(eastern Spain). Some BSC-forming species from gypsum soils suchas Acarospora placodiiformis (endangered), A. nodulosa var. reagens(vulnerable), Diploschistes diacapsis (lower risk), Fulgensia deserto-rum (vulnerable), F. poeltii (endangered), Lecidea circinarioides(endangered), Psora saviczii (endangered) are included in this list.Moreover, Aspicilia fruticulosa (endangered) and Heppia gigantea(vulnerable) are also included in this list. Guerra et al. (1995), ina study about the bryophyte and lichen flora of the gypsiferousoutcrops of SE Spain, pointed out that 17 lichen taxa are rare orendemic, living exclusively or almost exclusively on gypsum soils.

9. Importance of biological soil crust research in Spain andfuture research directions

The semi-arid ecosystems from Spain are an excellent fieldlaboratory to work with BSCs. Despite that these organisms havetraditionally been ignored, research carried out in this country hasbeen characterized by its originality, as topics poorly studiedworldwide have been tackled by scientists working in this country.These include species-specificity of BSC effects onplant germination(Escudero et al., 2007), the study of biotic interactions among BSCorganisms (Maestre et al., 2008, 2009a; Bowker et al., 2010a) and theuse of BSCs as model systems to explore ecosystem structure-functioning relationships (Bowkeret al., 2010b;Maestre et al., 2010).Biological soil crusts are proving to be an excellent model system tofoster new ways of thinking about key community and ecosystemecology topics. As an example, the greater number of species inter-actions possible under low stress conditions may render intransi-tivity (sensu Laird and Schamp, 2008) dominant over nichesegregation and expansion, potentially resulting in positive effectsof competition on species richness in low stress situations (Bowkeret al., 2010a). These results might not have been observed usinga vascular plant study system and highlights the utility of BSCs asamodel system for increasingour understandingof themechanismsstructuring biotic communities. In a similar direction, unlike othersoil communities, BSCs tend to exhibit linear non-saturatingdependencies of some ecosystem functions upon biodiversity(Maestre et al., 2010; Bowker et al., 2010b),illustrating the potentialof BSCs as a model system to explore the diversity-function rela-tionship between diversity and ecosystem functioning at severalspatial scales.

Although the advance in our knowledge of the ecological role ofBSCs in Spain has been enormous during the last ten years, muchremains to be learned from these organisms. Below we identifysome key research topics that deserve special research attention inthe future:



i) Roles of particular BSC species/traits on ecosystem functioning.Future studies should explicitly consider which particulartraits are underlying species and site-specific effects of BSCson nutrient cycling and soil water dynamics. The trait listsproposed for lichens, mosses and cyanobacteria/algae byBowker et al. (2010b) provides an excellent starting point totackle this issue.

ii) Interactions between BSC and other soil organisms. To date, nostudy has explored the effects of BSCs on key soil communi-ties such as nematodes, protozoa and soil mesofauna in Spain.This is an important gap in our knowledge that must beurgently filled by future research. Similar research effortsmust be carried out to study heterotrophic microbial pop-ulations associated to BSCs in Spain.

iii) Hydrological effects of BSCs. Information on the influence ofBSCs on rainfall interception, soil moisture, evaporation ordew deposition hardly exist for SE Spain, despite results fromother sites suggest their importance. Future studies shouldstudy in more detail the effects of BSCs on these componentsof the water balance at fine and coarser spatial scales.

iv) Ecosystem scale effects of BSCs on the C and N cycles. As esti-mations at the ecosystem scale based only on vegetated andbare ground areas can be rather conservative if the samplingeffort is not high enough to capture the spatial variability inthe C and N fluxes induced by BSCs, future studies shouldexplicitly consider the effects of BSCs when modeling andestimating C and N budgets at the ecosystem scale.

v) Restoration of BSCs. Promoting the recovery of BSC compo-nents is far from being integrated in current restorationpractitioner’s agenda. To fill this gap, pilot studies anddemonstration projects are needed to evaluate the potentialof current BSC restoration techniques.

We hope that this brief review will serve to illustrate thevariety and importance of the research carried out on SpanishBSCs during the last decades, and that it will stimulate otherresearch groups from Spain and abroad to start working withthese key organisms.

Acknowledgements

We thank Cristina Armas and three anonymous reviewers forcomments on a previous version of this manuscript. This reviewwas made possible thanks to the support of the European ResearchCouncil under the European Community’s Seventh FrameworkProgramme (FP7/2007-2013)/ERC Grant agreement n� 242658awarded to FTM. AE acknowledges support from the Remedinal2project, funded by Comunidad de Madrid. RL and YC acknowledgesupport from the Spanish Ministerio de Ciencia e Innovación(MICINN) and the European Regional Development Fund (ProjectPREVEA; CGL2007-63258/BOS), and from the Junta de Andalucía(Project COSTRAS; RNM- 3614). JC appreciates support fromMICINN (Program Consolider-Ingenio 2010; Project GRACCIE;CSD2007-00067) and Ministerio de Medio Ambiente y Medio Ruraly Marino (project RECUVES; 077/RN08/04.1). We would like tothank the Instituto Madrileño de Investigación y Desarrollo Rural,Agrario y Alimentario (IMIDRA) and the Viciana brothers forallowing us to work in land of their property at Aranjuez (Madrid)and Tabernas (Almería), respectively.

Appendix. Supplementary data

Supplementary data associated with this article can be found inonline version at doi:10.1016/j.jaridenv.2010.12.008.

References

Alexander, R.W., Calvo, A., 1990. The influence of lichens on slope processes in someSpanish badlands. In: Thornes, J.B. (Ed.), Vegetation and Erosion. J. Wiley &Sons, Chichester, pp. 385e398.

Anderson, D.C., Harper, K.T., Rushforth, S.R., 1982. Recovery of crytogamic soil crustsfrom grazing on Utah winter ranges. Journal Range Management 35, 355e359.

Armstrong, R.A., Welch, A.R., 2007. Competition in lichen communities. Symbiosis43, 1e12.

Atienza, V., Segarra, J.G., 2000. Preliminary Red list of the lichens of the Valenciancommunity (eastern Spain). Forest Snow and Landscape Research 75, 391e400.

Belnap, J., 2002. Nitrogen fixation in biological soil crusts from southeast Utah. USA.Biology and Fertility of Soils 35, 128e135.

Belnap, J., 2006. The potential roles of biological soil crusts in dryland hydrologiccycles. Hydrological Processes 20, 3159e3178.

Belnap, J., Eldridge, D., 2003. Disturbance and Recovery of Biological Soil Crusts. In:Belnap, J., Lange, O.L. (Eds.), Biological Soil Crusts: Structure, Function, andManagement. Springer-Verlag Berlin, Heidelberg, pp. 363e383.

Belnap, J., Hawkes, C.V., Firestone, M.K., 2003. Boundaries in miniature: twoexamples from soil. BioScience 53, 737e794.

Belnap, J., Lange, O.L., 2003. Biological Soil Crusts: Structure, Function, andManagement. Springer Verlag, Berlin.

Bevan, J.L., 2009. Dynamics of lichen dominated biological soil crusts in the ElCautivo badlands, Southeast Spain. PhD. Thesis, University of Liverpool, UK.

Bowker, M.A., 2007. Biological soil crust rehabilitation in theory and practice: anunderexploited opportunity. Restoration Ecology 15, 13e23.

Bowker, M.A., Maestre, F.T., Escolar, C., 2010b. Biological crusts as a model systemfor examining the biodiversity-ecosystem function relationship in soils. SoilBiology and Biochemistry 42, 405e417.

Bowker, M.A., Soliveres, S., Maestre, F.T., 2010a. Competition increases with abioticstress and regulates the diversity of biological soil crusts. Journal of Ecology 98,551e560.

Brooker, R.W., Maestre, F.T., Callaway, R.M., Lortie, C.L., Cavieres, L.A., Kunstler, G.,Liancourt, P., Tielbörger, K., Travis, J.M.J., Anthelme, F., Armas, C., Coll, L.,Corcket, E., Delzon, S., Forey, E., Kikvidze, Z., Olofsson, J., Pugnaire, F.I., Saccone, P.,Schiffer, K., Seifan, M., Touzard, B., Michalet, R., 2008. Facilitation in plantcommunities: the past, the present, and the future. Journal of Ecology 96,18e34.

Calder, E.A., 1959. Nitrogen fixation in a Uganda swamp soil. Nature 184, 746.Callaway, R.M., 2007. Positive Interactions and Interdependence in Plant Commu-

nities. Springer, New York.Calvo-Cases, A., Harvey, A.M., Paya-Serrano, J., Alexander, R.W., 1991. Response of

badlands surfaces in South East Spain to simulated rainfall. Cuaternario yGeomorfología 5, 3e14.

Cantón, Y., Domingo, F., Solé-Benet, A., Puigdefábregas, J., 2001. Hydrological anderosion response of a badlands system in semiarid SE Spain. Journal ofHydrology 252, 65e84.

Cantón, Y., Solé-Benet, A., Domingo, F., 2004. Temporal and spatial patterns of soilmoisture in semiarid badlands of SE Spain. Journal of Hydrology 285, 199e214.

Casares-Porcel, M., Gutiérrez-Carretero, L., 1993. Síntesis de la vegetación liquénicagipsícola termo- y mesomediterránea de la Península Ibérica. Cryptogamie.Bryologie et Lichénologie 14, 361e388.

Castillo-Monroy, A.P., Maestre, F.T., Delgado-Baquerizo, M., Gallardo, A., 2010. Bio-logical soil crusts modulate nitrogen availability in semi-arid ecosystems:insights from a Mediterranean grassland. Plant and Soil 333, 21e34.

Castillo-Monroy, A.P., Bowker, M.A., Maestre, F.T., Rodríguez-Echeverría, S., Martínez,I., Barraza-Zepeda, C.E., Escolar, C. Are the functional effects of biological soilcrusts mediated by the associated bacterial community? Insights from a semi-arid Mediterranean environment. Journal of Vegetation Science, in press.

Cerdá, A., 1997. The effect of patchy distribution of Stipa tenacissima L. on runoff anderosion. Journal of Arid Environments 36, 37e51.

Chamizo, S., Cantón, Y., Afana, A., Lázaro, R., Domingo, F., Solé-Benet, A., 2009. Howdevelopment and disturbance of biological soil crust do affect runoff anderosion in drylands? In: Romero-Díaz, A., Belmonte, F., Alonso, F., LópezBermúdez, F. (Eds.), Advances in Studies on Desertification. Servicio Pub-licaciones Universidad de Murcia EDITUM, Murcia, pp. 203e206.

Cortina, J., Maestre, F.T., Ramírez, D., 2009. Innovations in semiarid restoration. Thecase of Stipa tenacissima L. steppes. In: Bautista, S., Aronson and R, J., Vallejo(Eds.), Land Restoration to Combat Desertification. Innovative Approaches,Quality Control and Project Evaluation. Fundación CEAM, Valencia, pp. 121e144.

Cortina, J., Martín, N., Maestre, F.T., Bautista, S., 2010. Biological soil crusts havesmall effects on the performance of a key species in a semi-arid Mediterraneansteppe. Plant and Soil 334, 311e322.

Crespo, A., 1973. Composición florística de la costra de líquenes del Herniario-Teu-crietum pumili de la provincia de Madrid. Anales del Instituto Botánico AntonioJosé. Cavanilles 30, 57e68.

Crespo, A., Barreno, E., 1975. Ensayo florístico y ecológico de la vegetación liquénicade los yesos del centro de España (Fulgensietalia desertori ord. nov). Anales delInstituto Botánico Cavanilles 32, 873e908.

DeFalco, L.A., Detling, J.K., Richard Tracy, C., Warren, S.D., 2001. Physiological vari-ation among native and exotic winter annual plants associated with microbioticcrusts in the Mojave Desert. Plant and Soil 234, 1e14.

Delgado-Baquerizo, M., Castillo-Monroy, A.P., Maestre, F.T., Gallardo, A., 2010.Changes in the dominance of N forms within a semi-arid ecosystem. SoilBiology and Biochemistry 42, 376e378.



Del Prado, R., Sancho, L.G., 2007. Dew as a key factor for the distribution pattern ofthe lichen species Teloschistes lacunosus in the Tabernas Desert (Spain). Flora202, 417e428.

Deltoro, V.I., Calatayud, A., Gimeno, C., Barreno, E., 1998. Water relations, chloro-phyll fluorescence, and membrane permeability during desiccation in bryo-phytes from xeric, mesic, and hydric environments. Canadian Journal of Botany76, 1923e1929.

Eldridge, D.J., Bowker, M.A., Maestre, F.T., Alonso, P., Mau, R.L., Papadopolous, J.,2010. Interactive effects of three ecosystem engineers on infiltration in a sem-iearid Mediterranean grassland. Ecosystems 13, 499e510.

Escudero, A., Martínez, I., de la Cruz, A., Otálora, M.A.G., Maestre, F.T., 2007. Soillichens have species-specific effects on the seedling emergence of three gyp-sophile plant species. Journal of Arid Environments 70, 18e28.

García-Pichel, F., Pringault, O., 2001. Cyanobacteria track the water in desert soils.Nature 413, 380e381.

Goberna, M., Pascual, J.A., Garcia, C., Sanchez, J., 2007. Do plant clumps constitutemicrobial hotspots in semiarid Mediterranean patchy landscapes? Soil Biologyand Biochemistry 39, 1047e1054.

Gotelli, N.J., 2000. Null model analysis of species co-occurrence patterns. Ecology81, 2606e2621.

Grime, J. P, 2001. Plant Strategies, Vegetation Processes, and Ecosystem Properties,Second Edition. Wiley, Chichester, UK.

Guerra, J., Ros, R.M., Cano, M.J., Casares, M., 1995. Gypsiferous outcrops in SE Spain,refuges of rare, vulnerable and endangered bryophytes and lichens. Cryptoga-mie. Bryologie et Lichènologie 16, 125e135.

Hauck, M., Jürgens, S.-R., Willenbruch, K., Huneck, S., Leuschner, C., 2009. Dissoci-ation and metal-binding characteristics of yellow lichen substances suggesta relationship with site preferences of lichens. Annals of Botany 103, 13e22.

Hawkes, C.V., Menges, E.S., 2003. Effects of lichens on seedling emergence in a xericFlorida shrubland. Southeastern Naturalist 2, 223e234.

Laird, R.A., Schamp, B.S., 2008. Does local competition increase the coexistence ofspecies in intransitive networks? Ecology 89, 237e247.

Lange, O.L., 2003. Photosynthesis of Soil-crust Biota as Dependent on Environ-mental Factors. 2003. In: Belnap, J., Lange, O.L. (Eds.), Biological Soil Crusts:Structure, Function, and Management. Springer-Verlag, Berlin, pp. 217e240.

Lange, O.L., Kilian, E., Ziegler, H., 1986. Water vapor uptake and photosynthesis oflichens: performance differences in species with green and blue-green algae asphycobionts. Oecologia 71, 104e110.

Langhans, T.M., Storm, C., Schwabe, A., 2010. Regeneration processes of biologicalsoil crusts, macro-cryptogams and vascular plant species after fine-scaledisturbance in a temperate region: recolonization or successional replacement?Flora 205, 46e60.

Lázaro, R., Cantón, Y., Solé-Benet, A., Bevan, J., Alexander, R., Sancho, L.G.,Puigdefábregas, J., 2008. The influence of competition between lichen coloni-zation and erosion on the evolution of soil surfaces in the Tabernas badlands(SE Spain) and its landscape effects. Geomorphology 102, 252e266.

Llimona, X., 1974. Las comunidades de líquenes de los yesos de España. Universidadde Barcelona. Secretariado de Publicaciones, Barcelona.

Maestre, F.T., 2003a. Small-scale spatial patterns of two soil lichens in semi-aridMediterranean steppe. Lichenologist 35, 71e81.

Maestre, F.T., 2003b. Variaciones en el patrón espacial a pequeña escala de loscomponentes de la costra biológica en un ecosistema mediterráneo semiárido.Revista Chilena de Historia Natural 76, 35e46.

Maestre, F.T., Bautista, S., Cortina, J., Bellot, J., 2001. Potential of using facilitation bygrasses to establish shrubs on a semiarid degraded steppe. Ecological Appli-cations 11, 1641e1655.

Maestre, F.T., Cortina, J., 2002. Spatial patterns of surface soil properties andvegetation in a Mediterranean semi-arid steppe. Plant and Soil 241, 279e291.

Maestre, F.T., Huesca, M.T., Zaady, E., Bautista, S., Cortina, J., 2002. Infiltration,penetration resistance and microphytic crust composition in contrastedmicrosites within a Mediterranean semi-arid steppe. Soil Biology andBiochemistry 34, 895e898.

Maestre, F.T., Cortina, J., 2003. Small-scale spatial variation in soil CO2 efflux ina Mediterranean semiarid steppe. Applied Soil Ecology 23, 199e209.

Maestre, F.T., Cortina, J., 2004a. Are Pinus halepensis plantations useful as a resto-ration tool in semiarid Mediterranean areas? Forest Ecology and Management198, 303e317.

Maestre, F.T., Cortina, J., 2004b. Insights on ecosystem composition and function ina sequence of degraded semiarid steppes. Restoration Ecology 12, 494e502.

Maestre, F.T., Escudero, A., Martínez, I., Guerrero, C., Rubio, A., 2005. Does spatialpattern matter to ecosystem functioning? Insights from boilogical soil crusts.Functional Ecology 19, 566e573.

Maestre, F.T.,Martín,N., BeatrizDíez, B., López-Poma, R., Santos, F., Luque, I., Cortina, J.,2006. Watering, fertilization, and slurry inoculation promote recovery of bio-logical crust function in degraded soils. Microbial Ecology 52, 365e377.

Maestre, F.T., Escolar, C., Martínez, I., Escudero, A., 2008. Are soil lichen communitiesstructured by biotic interactions? A null model analysis. Journal of VegetationScience 19, 261e266.

Maestre, F.T., Martínez, I., Escolar, C., Escudero, A., 2009a. On the relationshipbetween abiotic stress and co-occurrence patterns: an assessment at thecommunity level using soil lichen communities and multiple stress gradients.Oikos 118, 1015e1022.

Maestre, F.T., Bowker, M.A., Puche, M.D., Hinojosa, M.B., Martínez, I., García-Palacios, P.,Castillo, A.P., Soliveres, S., Luzuriaga, A.L., Sánchez, A.M., Carreira, J.A., Gallardo, A.,Escudero, A., 2009b. Shrub encroachment can reverse desertification in Mediter-ranean semiarid grasslands. Ecology Letters 12, 930e941.

Maestre, F.T., Bowker, M.A., Escolar, C., Puche, M.D., Soliveres, S., Mouro, S., García-Palacios, P., Castillo-Monroy, A.P., Martínez, I., Escudero, A., 2010. Do bioticinteractions modulate ecosystem functioning along abiotic stress gradients?Insights from semi-arid Mediterranean plant and biological soil crust commu-nities. Philosophical Transactions of the Royal Society B 365, 2057e2070.

Martínez, I., Ecudero, A.,Maestre, F.T., de la Cruz, A., Guerrero, C., Rubio, A., 2006. Small-scale patterns of abundance ofmosses and lichens forming biological soil crusts intwo semi-arid gypsum environments. Australian Journal of Botany 54, 339e348.

Martínez-Sánchez, J.J., Casares, P.M.,Guerra, J., Gutiérrez,C.L., Ros,R.M.,Hernández, B.J.,Cano, M.J., 1994. A special habitat for bryophytes and lichens in the arid zones ofSpain. Lindbergia 19, 116e121.

Ministerio de Medio Ambiente, Rural y Marino, 2008. Programa de Acción Nacionalcontra la Desertificación. Ministerio de Medio Ambiente, Rural y Marino,Madrid.

Moro, M.J., Were, A., Villagarcía, L., Cantón, Y., Domingo, F., 2007. Dewmeasurementby Eddy covariance and wetness sensor in a semiarid ecosystem of SE Spain.Journal of Hydrology 335, 295e302.

Pintado, A., Sancho, L.G., Green, T.G.A., Blanquer, J.M., Lázaro, R., 2005. Functionalecology of the biological soil crust in semiarid SE Spain: sun and shade pop-ulations of Diploschistes diacapsis (Ach.) Lumbsch. Lichenologist 37, 425e432.

Pintado, A., Sancho, L.G., Blanquer, J.M., Green, T.G.A., Lázaro, R., 2010. Microclimaticfactors and photosynthetic activity of crustose lichens from the semiaridsoutheast of Spain: long-term measurements for Diploschistes diacapsis.Bibliotheca Lichenologica 105, 211e224.

Puigdefábregas, J., Solé-Benet, A., Gutiérrez, L., Del Barrio, G., Boer,M.,1999. Scales andprocesses of water and sediment redistribution in drylands: results from theRambla Honda field site in Southeast Spain. Earth-Science Reviews 48, 39e70.

Pugnaire, F., Armas, C., Valladares, F., 2004. Soil as a mediator in plant-plantinteractions in a semi-arid community. Journal of Vegetation Science 15, 85e92.

Rillig, M.C., Maestre, F.T., Lamit, L.J., 2003. Microsite differences in fungal hyphallength, glomalin, and soil aggregate stability in semiarid Mediterraneansteppes. Soil Biology and Biochemistry 35, 1257e1260.

Rivera-Aguilar, V., Godínez-Alvarez, H., Manuell-Cacheux, I., Rodríguez-Zaragoza, S.,2005. Physical effects of biological soil crusts on seed germination of two desertplants under laboratory conditions. Journal of Arid Environments 63, 344e352.

Ros, R.M., Guerra, J., 1997. Contribución a la flora y vegetación briofítica de losafloramientos de rocas volcánicas de la provincia de Albacete: la sierra de LasCabras. Al-Basit 40, 135e141.

Schaper, T., Ott, S., 2003. Photobiont selectivity and interspecific interactions inlichen communities. I. Culture experiments with the mycobiont Fulgensiabracteata. Plant Biology 5, 441e450.

Shreve, F.,1910. The rate of establishment of the giant cactus. PlantWorld 13, 235e241.Solé-Benet, A., Calvo, A., Cerdà, A., Lázaro, R., Pini, R., Barbero, J., 1997. Influences of

micro-relief patterns and plant cover on runoff related processes in badlandsfrom Tabernas (SE Spain). Catena 31, 23e38.

Soule, T., Anderson, I.J., Johnson, S.L., Bates, S.T., Garcia-Pichel, F., 2009. Archaealpopulations in biological soil crusts from arid lands in North America. SoilBiology and Biochemistry 41, 2069e2074.

Souza-Egipsy, V., Ascaso, C., Sancho, L.G., 2002. Water distribution within terrico-lous lichens revealed by scanning electron microscopy and its relevance in soilcrust ecology. Mycological Research 106, 1367e1374.

Souza-Egipsy, V., Wierzchos, J., Sancho, C., Belmonte, A., Ascaso, C., 2004. Role ofbiological soil crust cover in bioweathering and protection of sandstones ina semi-arid landscape (Torrollones de Gabarda, Huesca, Spain). Earth SurfaceProcesses and Landforms 29, 1651e1661.

Spitale, D., 2009. Switch between competition and facilitation within a seasonalscale at colony level in bryophytes. Oecologia 160, 471e482.

Tilman, D., 1988. Plant Strategies and the Dynamics and Structure of PlantCommunities. Princenton University Press, Princenton.

Warren, S.D., Eldridge, D.J., 2003. Biological soil crusts and livestock in aridecosystems: are they compatible? In: Belnap, J., Lange, O.L. (Eds.), Biological SoilCrusts: Structure, Function, and Management. Springer-Verlag, Berlin, Heidel-berg, pp. 363e383.

Yeager, C.M., Kornosky, J.L., Housman, D.C., Grote, E.E., Belnap, J., Kuske, C.R., 2004.Diazotrophic community structure and function in two successional stages ofbiological soil crusts from the Colorado Plateau and Chihuahuan Desert. Appliedand Environmental Microbiology 70, 973e983.

Zaady, E., Gutterman, Y., Boeken, B., 1997. The germination of mucilaginous seeds ofPlantago coronopus, Reboudia pinnata, and Carrichtera annua on cyanobacterialsoil crust from the Negev Desert. Plant and Soil 190, 247e252.


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