Unassisted establishment of biological soil crusts on dryland road … · 2020. 6. 4. · Laura...

Web Ecol 19 39ndash51 2019httpsdoiorg105194we-19-39-2019copy Author(s) 2019 This work is distributed underthe Creative Commons Attribution 40 License

Unassisted establishment of biological soil crusts ondryland road slopes

Laura Concostrina-Zubiri Juan M Arenas Isabel Martiacutenez and Adriaacuten EscuderoAacuterea de Biodiversidad y Conservacioacuten Departamento de Biologiacutea Geologiacutea Fiacutesica y Quiacutemica Inorgaacutenica

Universidad Rey Juan Carlos Moacutestoles 28933 Madrid Spain

Correspondence Laura Concostrina-Zubiri (lauraconcostrinaurjces) and Juan M Arenas(juanmariaaegmailcom)

Received 13 January 2019 ndash Revised 12 May 2019 ndash Accepted 15 May 2019 ndash Published 6 June 2019

Abstract Understanding patterns of habitat natural recovery after human-made disturbances is critical for theconservation of ecosystems under high environmental stress such as drylands In particular the unassisted estab-lishment of nonvascular plants such as biological soil crusts or biocrust communities (eg soil lichens mossesand cyanobacteria) in newly formed habitats is not yet fully understood However the potential of biocrusts toimprove soil structure and function at the early stages of succession and promote ecosystem recovery is enor-mous In this study we evaluated the capacity of lichen biocrusts to spontaneously establish and develop on roadslopes in a Mediterranean shrubland We also compared taxonomic and functional diversity of biocrusts betweenroad slopes and natural habitats in the surroundings Biocrust richness and cover species composition and func-tional structure were measured in 17 road slopes (nine roadcuts and eight embankments) along a 13 km highwaystretch Topography soil properties and vascular plant communities of road slopes were also characterized Weused KruskalndashWallis tests and applied redundancy analysis (RDA) to test the effect of environmental scenario(road slopes vs natural habitat) and other local factors on biocrust features We found that biocrusts were com-mon in road slopes after sim 20 years of construction with no human assistance needed However species richnessand cover were still lower than in natural remnants Also functional structure was quite similar between roadcuts(ie after soil excavation) and natural remnants and topography and soil properties influenced species composi-tion while environmental scenario type and vascular plant cover did not These findings further support the ideaof biocrusts as promising restoration tools in drylands and confirm the critical role of edaphic factors in biocrustestablishment and development in land-use change scenarios

1 Introduction

Biological soil crusts (biocrusts) have earned a place as keyecosystem components in drylands in the last decades (We-ber et al 2016a) They are complex communities composedof lichens bryophytes fungi cyanobacteria and other mi-croorganisms living on and interacting with the first soillayers and are found in almost every dryland occurring instressful conditions ie water scarcity and high solar radia-tion and temperatures Biocrusts contribute greatly to ecosys-tem diversity with several tens of species per square me-tre and to ecosystem functioning being critical in the fix-ation of carbon and nitrogen (Elbert et al 2012) controllingtopsoil structure (Jimenez Aguilar et al 2009) chemistry

(Delgado-Baquerizo et al 2015) and hydrology (Chamizo etal 2013) and also modulating biotic interactions (Luzuriagaet al 2012) Moreover due to the functional roles they per-form and their ability to establish and develop in very harshenvironments biocrusts have been pointed out as promis-ing tools in dryland restoration (Bowker 2007) Some of thebiocrust constituents are early fast colonizers of degraded ar-eas with enormous potential to aid and speed up ecosystemstructure and functioning recovery eg stabilizing soil sur-face improving soil fertility maintaining soil humidity andpromoting the establishment of vascular plants (Weber et al2016a) This is particularly true in strongly disturbed areasunder high abiotic stress where vascular plant development

Published by Copernicus Publications on behalf of the European Ecological Federation (EEF)

40 L Concostrina-Zubiri et al Biocrusts on dryland road slopes

is less likely to occur due to a higher demand on soil re-sources and lower tolerance of water scarcity among others(Bowker 2007)

Biocrusts have been shown to recover naturally withoutassistance from mechanical disturbances such as grazingtrampling and vehicle driving and also from fire at varyingrecovery rates and following different community trajecto-ries depending on the disturbance type intensity and timing(Belnap and Eldridge 2003) However little is known aboutnatural recovery of biocrusts in newly formed and emer-gent habitats such as those generated after the constructionof linear infrastructures which include massive soil removalor the accumulation of exogenous soil material At the veryfine spatial scale (ie topsoil area lt 10 m2) several studieshave evaluated biocrust natural colonization and establish-ment after biocrust removal (ie scalping) Recovery ratesrange from less than 3 years for cyanobacteria commonlythe earliest fastest colonizers within biocrusts up to a fewdecades or almost a millennium for bryophytes and lichensthe typical components of more developed mature biocrusts(reviewed in Weber et al 2016b) Similarly to biocrust re-covery in secondary succession the colonization and estab-lishment of biocrusts largely depend on climate particularlyprecipitation amount and timing after disturbance and soilproperties such as soil stability and nutrient concentration(Weber et al 2016b)

Surprisingly to our knowledge there is only one studyfocusing entirely on the recovery of biocrust communitieson road slopes (Chiquoine et al 2016) Yet Chiquoineet al (2016) did not focus on natural colonization but onsuccessful establishment after applying biocrust inoculumamong other restoration treatments This is a bit strikingsince there is no baseline for comparison Therefore noprevious study has evaluated the unassisted recovery ofbiocrusts on road slopes and this limited knowledge onbiocrust recovery under natural conditions weakens manyprojects of ecological restoration of road slopes in drylands

In contrast many studies have highlighted the role of nat-ural colonization in the establishment of vascular vegeta-tion on road slopes (Bochet et al 2007 Mola et al 2011Arenas et al 2017a b) In Mediterranean drylands na-tive vascular plants can establish and develop well in roadslopes in the absence of human assistance when the slope isgentle (lt 45) (Bochet and Garciacutea-Fayos 2004) and suffi-cient propagule is available from the surroundings (Arenaset al 2017b) However species composition differs notablyfrom communities found in the natural surrounding areasmainly due to topography and modification of initial soilconditions derived from the process of road slope construc-tion (Bochet and Garciacutea-Fayos 2004 Arenas et al 2017a)Moreover within road slopes roadcuts and embankmentshave very different structural properties (eg soil removalvs soil application respectively) and environmental char-acteristics and as a result further differences can be foundbetween their respective plant communities at the compo-

sitional level (Arenas et al 2017a) For biocrusts we ex-pect to find processes of colonization and community as-sembly on road slopes similar to those that occur for vas-cular vegetation and therefore evidence the ecological in-terest of natural colonization as a useful biocrust restora-tion measure In particular we hypothesized that biocrustsestablish easily in the road slopes provided that biocrustsare common and abundant in the surroundings (ie inocu-lum availability) and because of their capacity to tolerateharsh environmental conditions typical for newly createdhabitats (eg very thin soil high radiation inputs) (Weberet al 2016b) Nevertheless we expect to find marked differ-ences in biocrust composition depending on road slope type(ie roadcut vs embankment) topography soil propertiesand vascular plant abundance since the diversity of these or-ganisms is highly sensitive to changes in (i) climate at thelocal and microscale given by topography eg sun vs shadeenvironments (Pintado et al 2005) (ii) soil physicochemicalproperties eg texture (Fischer and Subbotina 2014) nutri-ent content (Bowker et al 2006) and pH (Ochoa-Hueso etal 2011) and (iii) biotic interactions especially with vascu-lar plants eg biocrustndashplant facilitationndashcompetition pro-cesses (reviewed in Bowker et al 2016) In this study weaimed to assess the potential of lichen biocrusts to colonizeand prosper in pioneer habitats under natural conditions (iewith no artificial assistance) We focused only on lichens be-cause they are the most conspicuous rich and common com-ponents of biocrusts in Mediterranean grasslands and shrub-lands (Concostrina-Zubiri et al 2014) even in fragmentedlandscapes (Concostrina-Zubiri et al 2018)

Specifically we addressed the following questions (1) canlichen biocrusts establish on road slopes spontaneously Ifso (2) what species and functional attributes characterizethe newly formed communities Regarding the functionalattributes characterizing these communities we focused oneutrophication tolerance gypsum tolerance because ourbiocrust model occurs in this type of soil (Concostrina-Zubiriet al 2018) and thallus continuity to test the following hy-potheses (i) lichen biocrust communities in the road slopesare more tolerant to high nutrient levels (eg derived fromthe road traffic and the subsequent passive air fertilization)(ii) they present a higher tolerance ofaffinity to gypsum con-tent as expected in a less developed topsoil layer at roadslopes compared to natural remnants where soil carbon andother nutrients had higher levels (Arenas et al 2017a) and(iii) lichen biocrusts with a less continuous thallus are morelikely to colonize and prosper in road slopes characterizedby a more hostile microenvironment (3) What is the roleof habitat scenario type (eg road slopes vs natural areas)and other local factors (ie topography soil properties andvascular plant communities) in determining the structure andcomposition of lichen biocrusts By addressing these ques-tions we could identify the factors that determine the naturalcolonization of biocrust in road slopes and point out somerestoration measures to carry out in road slopes for promot-

Web Ecol 19 39ndash51 2019 wwwweb-ecolnet19392019

L Concostrina-Zubiri et al Biocrusts on dryland road slopes 41

Figure 1 Map of the study area showing the road (in black)roadcuts (squares) embankments (circles) and natural remnants (ingrey)

ing the natural recovery of biocrusts Beyond road restora-tion this information is critical to the progress of current re-search on artificial recovery of biocrusts a growing body ofwork in the last years

2 Material and methods

21 Study area

This study was conducted in the road slopes and surround-ing natural habitat remnants of a typical Mediterranean gyp-sum shrubland in central Spain The study area comprisedtwo adjacent rectangles each 3 km wide along both sidesof a 13 km segment of the A3 national highway (Fig 1)between Fuentiduentildea del Tajo (407prime796primeprime N 39prime4196primeprimeW570 m asl) and Belinchoacuten (402prime5295primeprime N 33prime2968primeprimeW761 m asl) The highway goes through an extensive land-scape of cereal croplands where small patches of naturalvegetation remain The vegetation in these natural patchesis characterized by an open shrubland dominated by gypso-phytes such as Thymus lacaitae Pau Lepidium subulatum Land Helianthemum squamatum (L) Dum Cours accompa-nied by perennial grasses such as Stipa tenacissima L andKoeleria castellana Boiss amp Reut among others Soils arepredominantly Typic Gypsiorthid (gt 70 gypsum soil con-tent) The climate in the area is Mediterranean semiarid witha mean annual precipitation of 443 mm and mean annualtemperature of 14 C with a very intense summer drought(Ninyerola et al 2005)

22 Biocrust sampling and identification

We selected 17 road slopes along the 13 km highway stretchand differentiated two types because of big differences in

their structural and physicochemical properties (i) roadcuts(n= 9) which are constructed by excavation resulting in ar-eas of bare soil and exposed bedrock and (ii) embankments(n= 8) which are constructed by heaping and compactingmaterials and eventually receiving topsoil treatments (Tormoet al 2009) At each road slope we established a centralsampling plot (240 mtimes 240 m) and regularly divided it in64 quadrats (30 cmtimes 30 cm cells) Then we randomly se-lected 10 quadrats to estimate lichen biocrust species abun-dance visually as the percentage cover per species We alsosampled lichen biocrust communities in natural habitat rem-nants adjacent to the highway to compare lichen biocrustcommunities colonizing the emergent habitats (road slopes)to natural well-established lichen biocrusts To do so we se-lected 50 natural shrubland remnants immersed in an agri-cultural matrix in a ca 76 km2 area comprising two ad-jacent 3 km rectangles at both sides of the 13 km stretchof the national motorway (Fig 1) Then we followed thesame sampling design for each remnant as in the road slopes(see Concostrina-Zubiri et al 2018 for more details of thestudy system) We focused only on lichen biocrusts becausethey are the most conspicuous rich and common compo-nents of Mediterranean biocrusts (Concostrina-Zubiri et al2014 2018) and allowed a relatively easy identification inthe field Other typical biocrust organisms such as cyanobac-teria and mosses were not considered in this study althoughthey were present in the road slopes but marginally or notvisually apparent (personal observation) Lichen biocrustswere identified to the species level when possible follow-ing Nimis and Martellos (2016) and Prieto et al (2010a b)for Placidium We collected lichen specimens of species thatcould not be identified to the species level in the field foridentification in the laboratory We identified a total of 18taxa 15 lichens and three lichen groups identified in thefield as Enchylium complex (dominated by E tenax (Sw)Gray E coccophorum (Tuck) Otaacutelora P M Joslashrg amp Wedinand Blennothallia crispa (Hudson) Otaacutelora P M Joslashrg ampWedin) Gyalolechia complex (including G fulgens (Sw)Soslashchting Froumldeacuten amp Arup and G subbracteata (Nyl) Soslashcht-ing Froumldeacuten amp Arup) and Placidium complex (dominatedby P squamulosum (Ach) Breuss P pilosellum (Breuss)Breuss and Clavascidium lacinulatum (Ach) M Prieto)Lichen biocrusts are referred to hereafter as ldquobiocrustsrdquo andspecies and species complexes are referred to as ldquospeciesrdquofor simplicity Nomenclature follows Hladun and Llimona(2002ndash2007) and Prieto et al (2010a b) except Clavascid-ium lacinulatum (Ach) M Prieto which follows Prieto etal (2012) Enchylium spp which follow Otaacutelora et al (2014)and Gyalolechia spp which follow Arup et al (2013)

23 Characterization of biocrust communities

We characterized biocrust communities by measuring totalcover (ie mean percentage cover) species richness (iemean number of biocrust species sl) species composition

wwwweb-ecolnet19392019 Web Ecol 19 39ndash51 2019


and functional structure at each plot To assess functionalstructure we first classified each species considering differ-ent ecological features ie eutrophication tolerance gyp-sum tolerance and thallus continuity (Table 2) The eutroph-ication tolerance of biocrusts was classified into two cate-gories following Nimis and Martellos (2017) (1) speciesnot resistant to eutrophication or resistant to very weak eu-trophication (low) (2) species resistant to weak eutrophica-tion (medium) The gypsum tolerance of each species wasclassified into three categories following Concostrina-Zubiriet al (2014) and field observations (1) species that are rarelyfound on gypsum soils (low) (2) species that are less abun-dant on gypsum soils compared to other substrates (medium)(3) species generally growing on gypsum soils only (high)The thallus continuity was classified into three classes fol-lowing Nimis and Martellos (2017) and field observations(1) thallus consisting of disperse squamules or with a fru-ticose morphology (discontinuous) (2) thallus with moreor less contiguous squamuleslobes or with a foliose mor-phology (semicontinuous) and 3) thallus with a crustosendashplacodioidndashleprose morphology (continuous) Complexes in-cluding several species (ie Enchylium Gyalolechia andPlacidium complexes sl) were classified as the common cat-egory for the species constituting the complexes (ie all ormost of the species in the complex shared the same functionalcategory as for Enchylium and Gyalolechia complexes) or asthe category for the most abundant species in gypsum soils(following Concostrina-Zubiri et al 2014 and field observa-tions as for Placidium complex) Secondly we evaluated thefunctional structure of biocrust communities at each plot cal-culating the eutrophication tolerance index the gypsum tol-erance index and the thallus continuity index by means of thecommunity-weighted mean (CWM) for each ecological fea-ture CWMs were adapted for each multinomial functionalvariable For instance we calculated eutrophication tolerance(ET) of each plot by using the following index (1)

ET=nsum

sp=1ETsplowastCoversp

nsumsp=1

Coversp (1)

where ETsp is the eutrophication tolerance of each species(low medium) Coversp is the estimated cover of each speciesand n is the species richness in each plot ET can range be-tween 1 (all species of a plot show low tolerance) and 2 (allspecies show medium tolerance) The CWM for gypsum tol-erance (GT) or thallus continuity (TC) was estimated in thesame way as ET replacing ETsp by GTsp or TCsp with bothpresenting three levels low (value= 1) medium (value= 2)and high (value= 3) for GTsp and discontinuous (value= 1)semicontinuous (value= 2) and continuous (value= 3) forTCsp Therefore GT and TC can range between 1 and 3

24 Characterization of road slope topography soilproperties and vascular plant communities

In order to partial out the effect of topography soil variabil-ity and vascular plants in each plot (on both road slopes andnatural remnants) we first measured the slope aspect andlatitude in the center of the plot for calculating the heat loadindex (McCune and Keon 2002) The heat load index canbe regarded as a measure of potential solar radiation sym-metrical about the northndashsouth axis and is expected to influ-ence biocrust establishment and development via soil tem-perature and moisture modification among others (Bowkeret al 2016) Then soil properties were characterized bycollecting one soil sample (5 cm diameter and 10 cm deep)under dominant perennial plants (ldquoplant micrositerdquo) in eachplot Also another sample was collected from areas devoidof plant cover (ldquointerspace micrositerdquo) which are typicallycovered with biocrusts These samples were collected in Au-gust when the soil was dry Samples were analyzed for totalorganic C (OC) total N total P K pH electrical conductiv-ity (EC) and two soil enzyme activities related to C dynam-ics (β-glucosidase) and P (acid phosphatase) cycles Labo-ratory techniques used to determine each soil parameter areexplained in Appendix S1 Soil stoniness was also estimatedas the percentage cover of rock or rock fragmentsgt 10 cm ineach plot Finally the percentage cover of perennial plants(plant cover hereafter) in each plot was sampled in a parallelstudy (Arenas et al 2017a) by visual estimation Taking intoaccount the plant cover and the bare ground surface of eachplot we calculated a weighted averaged mean value per soilvariable considering the samples collected at the plant andinterspace microsites Average values (plusmn SE) for topographyvariables soil properties and plant cover at each environmen-tal scenario are shown in Table 3

25 Data analyses

To test for differences in total biocrust cover species richnessand CWM for the three functional indices (ie eutrophica-tion tolerance gypsum tolerance and thallus continuity) be-tween environmental scenarios (ie embankments roadcutsand remnants or roadcuts vs remnants) we conducted non-parametric KruskalndashWallis tests and when significant differ-ences were found we used the ConoverndashIman test for posthoc analyses For total biocrust cover and species richnesswe included all plots (ie eight embankments nine roadcutsand 50 natural remnants) However to calculate the CWMfor the three functional indices we only included plots wherelichen biocrust communities and more than one species werepresent (McCune and Grace 2002) Therefore we limitedthe analysis to six roadcuts and the 50 natural remnantswhile embankments were excluded (ie only one specieswas found in this scenario type) Analyses were performedusing the ldquokruskal()rdquo function in the agricolae R package (de



Table 1 Biocrust species codes and frequency as number and percentage of plots at each scenario For roadcuts and embankments twopercentages are presented the first is relative to the total number of plots for each scenario and the second is relative only to the number ofplots where biocrusts were present in brackets

Species Code Embankments Roadcuts Natural remnants

No No No

Acarospora nodulosa var reagens AcNo 0 0 0 0 12 024Acarospora placodiiformis AcPla 0 0 0 0 7 014Buellia zoharyi BuZo 0 0 0 0 2 004Cetraria aculeata CeAc 0 0 0 0 4 008Cladonia convoluta ClaCo 0 0 2 022 (033) 30 060Diplotomma alboatrum DiAl 0 0 0 0 14 028Diploschistes diacapsis DiDi 0 0 1 011 (016) 34 072Enchylium complex EnCo 5 062 (1) 6 067 (1) 49 098Gyalolechia complex GyCo 0 0 6 067 (1) 48 096Leproloma sp LeSp 0 0 1 011 (016) 12 024Placidium complex PlaCo 0 0 4 044 (067) 47 094Placynthium nigrum PlaNi 0 0 2 022 (033) 18 036Psora decipiens PsoDe 0 0 0 0 44 088Psora globifera PsoGl 0 0 0 0 5 010Psora savizcii PsoSa 0 0 0 0 19 038Squamarina cartilaginea SqCa 0 0 0 0 7 014Squamarina lentigera SqLe 0 0 0 0 38 076Toninia sedifolia ToSe 0 0 2 022 (033) 45 090

Table 2 Biocrust species and functional trait categories See Ta-ble 1 for species codes

Eutrophication Gypsum ThallusCode tolerance tolerance continuity

AcNo Low High ContinuousAcPla Low High ContinuousBuZo Low High SemicontinuousCeAc Low Low DiscontinuousClaCo Low Medium SemicontinuousDiDi Medium Medium ContinuousDiEp Medium High ContinuousEnCo Medium Medium SemicontinuousGyCo Medium Medium SemicontinuousLeSp Low High ContinuousPlaCo Medium Medium SemicontinuousPlaNi Medium Low ContinuousPsoDe Medium Medium SemicontinuousPsoGl Low High SemicontinuousPsoSa Low Medium SemicontinuousSqCa Medium Medium ContinuousSqLe Low Medium ContinuousToSe Medium Medium Semicontinuous

Mendiburu 2017) The Bonferroni correction was used toadjust p values for multiple comparisons

The relative importance of the type of environmental sce-nario on biocrust composition (ie species abundance persite matrix) was evaluated using redundancy analysis (RDA)

RDA is a linear ordination method like principal componentanalysis where the response variables (ie species com-position) are modeled as a function of explanatory or con-straining variables (ie environmental variables Zuur et al2007) There are as many RDA axes (ldquoconstrained axesrdquo) asthere are continuous explanatory variables or (nminus1) levels innominal explanatory variables Once all possible RDA axeshave been calculated a series of principal component anal-ysis (PCA) axes are calculated to maximize the explanationof the remaining variation in the data (ldquounconstrained axesrdquo)In our case we limited the RDA to roadcuts and natural rem-nant scenarios where biocrusts and more than one specieswere present (6 and 50 plots respectively) as for CWM Thismeans we only used a nominal variable with two levels andthus only one RDA axis was calculated followed by PCAaxes Because Euclidean distance (used in RDA) is inappro-priate for raw species abundance data involving many zerovalues the species abundance matrix was transformed us-ing the Hellinger standardization (Legendre and Gallagher2001) RDA was performed using the ldquorda()rdquo function inthe vegan R package (Oksanen et al 2018) Then to ex-amine if topography soil properties and plant cover influ-enced the composition of biocrust communities the afore-mentioned groups of variables were fitted to the RDA sep-arately and their significance was tested using the ldquoenvfit()rdquofunction in the vegan R package (Oksanen et al 2018) Fi-nally three partial RDAs were conducted to determine therelative importance of the type of environmental scenario af-ter removing the effect of topography soil and plant cover



Table 3 Average values (plusmn SE) for topography soil properties and plant cover at each scenario For each variable the significance value ofthe corresponding KruskalndashWallis test is given Different letters indicate significant differences (ConoverndashIman test for post hoc comparisonsp lt 005)

Variable p Embankments Roadcuts Natural remnants

Topography

Slope () 0000 3075plusmn 372 a 4283plusmn 241 a 752plusmn 045 b

Heat load 0460 085plusmn 008 a 069plusmn 010 a 093plusmn 001 a

Soil property

β-glucosidase(micromol PnP gminus1 hminus1) 0004 323plusmn 055 a 156plusmn 032 ab 135plusmn 010 b

Acid phosphatase(micromol PnP gminus1 hminus11) 0167 073plusmn 016 a 057plusmn 007 a 051plusmn 004 a

N () 0000 206plusmn 049 ab 126plusmn 021 b 269plusmn 015 a

P (mg kgminus1) 0501 051plusmn 009 a 038plusmn 009 a 041plusmn 003 a

K (ppm) 0006 012plusmn 003 ab 013plusmn 004 a 005plusmn 000 b

OC () 0000 158plusmn 036 ab 083plusmn 015 b 208plusmn 011 a

pH 0006 800plusmn 006 a 777plusmn 006 ab 775plusmn 003 b

EC (dS mminus1) 0002 072plusmn 029 b 189plusmn 008 a 164plusmn 008 a

Stoniness () 0000 825plusmn 322 a 2644plusmn 1086 a 230plusmn 091 b

Plant cover () 0540 3875plusmn 719 a 2900plusmn 613 a 3224plusmn 202 a

separately The partial RDAs were carried out using the ldquordardquofunction in the vegan R package The significance (Type IIIANOVA) of the RDA and the partial RDAs was analyzedusing permutation tests with 999 randomizations using theldquoanovacca()rdquo function in the vegan R package (Oksanen etal 2018) All statistical analyses were performed using the Rsoftware version 351 (httpcranr-projectorg last access1 December 2018)

3 Results

Biocrusts were naturally present in about two-thirds of boththe embankments (five out of eight) and roadcuts (six out ofnine Table 1) We found a total of eight biocrust species inroad slopes all of them were present in the roadcuts but onlyone (ie Enchylium complex) in the embankments (Table 1)The total number of biocrust species in natural areas was 18including those present in road slopes We also found onelichen species in natural areas with a very poorly developedthallus that could not be identified and it was then discardedfor further analysis in this study The most frequent species inthe roadcuts were Enchylium complex and Gyalolechia com-plex both present in six out of nine plots (Table 1) Addi-tionally Gyalolechia complex had the highest mean cover inthe roadcut scenario (gt 1 ) Leproloma sp had the maxi-mum cover recorded in the roadcuts (ca 10 ) although thisspecies was present in only one plot at this scenario type (Ta-ble 1) Enchylium complex was the only species found in theembankments present in five out of our plots (Table 1) andwith a maximum recorded cover of 2

Figure 2 Average values (plusmn SE) for biocrust richness and coverRs-Em embankments Rs-Rc roadcuts Nr natural remnants Foreach graph the significance value of the KruskalndashWallis test isgiven Different letters indicate significant differences (ConoverndashIman test for post hoc comparisons p lt 005) among environmen-tal scenarios

Species richness showed a tendency to increase in the fol-lowing order embankmentslt roadcutslt natural remnantsHowever this variable was statistically similar in the em-bankments and roadcuts (mean species richness of 06 and27 respectively) while it increased significantly (up to 88)in the natural remnants (Fig 2a) Similarly total biocrustcover was significantly lower in the embankments and road-cuts (ca 1 and 5 respectively) compared to the naturalremnants (ca 12 Fig 2b)

The CWM for eutrophication and gypsum tolerancewas similar in roadcuts and natural remnants (p gt 0050Fig 3a b) while CWM for thallus continuity was signifi-cantly lower in the roadcuts compared to the natural remnants(Fig 3c)



Figure 3 CWMs (plusmn SE) for eutrophication tolerance (ldquoeutrophtolerancerdquo) gypsum tolerance and thallus continuity Rs-Rc road-cut Nr natural remnants The significance value of the KruskalndashWallis test is given for each graph Different letters indicate sig-nificant differences (ConoverndashIman test for post hoc comparisonsp lt 005) among environmental scenarios

The RDA of biocrust composition using the type of sce-nario as the constraining variable showed a clear separa-tion of roadcuts towards the positive end of the RDA1 axisfrom natural remnants Also biocrust composition was sig-nificantly correlated to OC EC K slope acid phosphatasestoniness and heat load (Fig 4a) The characteristic specieswith centroids at this positive extreme were Enchylium com-plex Gyalolechia complex Leproloma sp and Placidiumcomplex (results not shown) The type of scenario (road-cuts vs natural remnants) significantly explained (F = 351p = 0001) 61 of variance of the RDA (Fig 4a) How-ever after removing the variation given by topography andsoil variables the partial RDAs (Fig 4b and c) were not sig-nificant (F = 096 p = 0440 and F = 075 p = 0630 re-spectively) In contrast the partial RDA after removing thevariation given by plant cover (Fig 4d) remained significant(F = 368 p = 0002)

4 Discussion

Previous work on unassisted revegetation of newly createdhabitats has mostly focused on vascular plants while the re-covery of biocrust communities has been disregarded More-over to our knowledge this is the first study assessing nat-ural recovery of biocrusts (ie unassisted) in road slopesOur results showed that biocrusts can colonize and establishon road slopes particularly after soil excavation (ie as inroadcuts) Surprisingly biocrust communities developed onroadcuts were relatively similar in composition to those onsome natural remnants Moreover we found that topogra-phy and fine-scale soil properties were more important thanthe type of environmental scenario (ie roadcuts vs naturalremnants) in determining biocrust species composition Nev-ertheless our results suggest that the scenario type may exertsome influence on biocrust establishment and developmentmediated by the vascular plant community configuration as-sociated with each scenario

41 Natural recovery of biocrusts on new habitats

Although some biocrust components such as cyanobacte-ria algae and even mosses are regarded as early coloniz-ers in primary succession (Belnap and Eldridge 2003) lit-tle is known about their potential to colonize and estab-lish in newly created habitats without human assistanceFor example biocrusts (including lichens and mosses) werefound to be the dominant life form in the first 100 m after10 years of glacier retreat in a Canadian deglaciated val-ley (Breen and Leacutevesque 2008) and widespread communi-ties after sim 20 years of lava flows (Jackson 1971) How-ever only a couple of studies have assessed biocrust colo-nization and establishment in human-made habitats Gypseret al (2016 2015) evaluated the structural and functional de-velopment of biocrusts in post-mining sites in German dry-lands These authors found that 13ndash23 years after miningactivity cessation biocrust communities were able to colo-nize the new substrate mostly composed of applied tertiaryand quaternary materials initially as green algaendashmoss com-munities and developing into rich and extensive mossndashlichencarpets over years (Gypser et al 2016 2015) Also Gypseret al (2015) reported an increase in biocrust NDVI (nor-malized difference vegetation index) and chlorophyll fluo-rescence with biocrust developmental state evidencing thefunctional recovery of these communities in a relatively shorttime (ie lt 20 years) Similarly our results showed thatlichenndashbiocrusts can recover naturally as fast as 20 yearsafter habitat creation ie approximate date of road slopeconstruction but only in roadcuts It is worth noting that al-though almost half of the species present in natural remnantswere found in roadcuts biocrust richness and cover were stillnotably lower than in natural remnants Nevertheless theseresults contrast with estimated recovery rates for biocrustsin a machine-cleared road scenario (Lalley and Viles 2008)which ranged from the multi-decade to the multi-centuryscale The great differences in recovery times are likely dueto climate semiarid vs hyper-arid in the case of Lalley andViles (2008) but also to the availability and proximity ofbiocrust inoculum Actually when topsoil surface is removedat fine scales eg as in scalped patches of less than 1 m2 andimmediately surrounded by biocrust material biocrust recov-ery can be as fast as 3 years for cyanobacteria or lower than5 years for bryophytes (Dojani et al 2011 Tian et al 2006)In our study remnants of natural habitat with well-developedbiocrusts are only a few metres apart from the road slopeswhich may have favored and speeded up the colonizationprocess at our study scale (ie sufficient biocrust inoculumavailability)



Figure 4 (a) RDA using the type of scenario as the constrainingvariable (b c d) Partial RDAs using the type of scenario as theconstraining variable in which the variation attributable to (b) to-pography (c) soil and (d) plant cover was removed before adjustingthe model RDA ordination plots are based on the first and onlyRDA axis (RDA1) and the following most explanatory PCA axis(PCA1) Variables that significantly adjust to the RDA (p lt 005)are represented by arrows

42 Biocrust structure and composition acrossenvironmental scenarios are mostly driven bytopography and edaphic factors

Our results also showed that biocrust richness and cover werenotably lower in road slopes than in adjacent natural areasand that the newly established communities were character-ized by a lower thallus continuity CWM Moreover strik-ing differences between roadcuts and embankments werefound in terms of species number Specifically only onespecies Enchylium complex was found on embankmentswhile roadcuts and natural remnants had a total of 8 and 18species respectively Firstly these results are likely due tothe typically marked structural dissimilarities between em-bankments and roadcuts (Arenas et al 2017a Jimenez etal 2011) although the studied soil properties were gener-ally similar in these scenario types Roadcuts are constructedby excavation generating areas of exposed bedrock and baresoil while embankments are constructed by heaping andcompacting material and generally applying topsoil treat-ments (Tormo et al 2009) The artificially created topsoilin the embankments is likely to limit the number of biocrustspecies able to colonize and establish in these scenarios be-cause among the potential edaphic factors responsible forbiocrust establishment soil stability has been widely recog-nized as one of the most relevant In particular older soils

embedded and shallower (more stable) at roadcuts are likelyto promote a faster recovery of biocrusts (Belnap and El-dridge 2003) Conversely soil structure and age may alsoexplain the presence of only one species Enchylium com-plex in the embankments where less stable younger anddeeper soils formed by applied materials may dominate Nev-ertheless Enchylium spp have been identified as early suc-cessional biocrust species (Belnap and Eldridge 2003) andplay an important ecological role in the development of newhabitats the photobiont of these lichens is a cyanobacteriaable to fix N and thus contribute to the improvement of soilproperties for the next successional stages

Although we did not characterize soil texture this soilproperty has been found to be different in roadcuts and em-bankments in other road slopes ie roadcuts have coarsersoils than embankments (Jimenez et al 2011) Indeed soilstoniness in roadcuts tended to be higher than in embank-ments in our study area This may have benefited biocrustdevelopment because scattered rocks or rock fragments canact as microclimatic shelters (eg reducing solar radiation)and as nutrient and biocrust inoculum traps among others(Bowker et al 2016) Additionally we found no significantdifferences in topography between embankments and road-cuts but slope values tended to be higher in the roadcut sce-nario Steeper slopes and coarser soils typically found inroadcuts may explain the generally lower plant cover in thisscenario type due to the potential difficulty for seeds to estab-lish and grow (Bochet and Garciacutea-Fayos 2004) or the lowerwater availability (Jimenez et al 2011) among other fac-tors In turn vascular plant cover can also be determinant inbiocrust establishment and development

On the one hand it is generally accepted that biocrustcommunities are more abundant and diverse in open ecosys-tems with sparse plant cover (Bowker et al 2016) wherecompetition for space is lower On the other hand the morebenign microclimate created by plants (eg lower solar ra-diation higher humidity) in drylands can benefit biocrustphysiological performance (Hui et al 2013 Niemi et al2002 Singh et al 2012) although shaded vs open environ-ment preference can be highly species-specific (Concostrina-Zubiri et al 2014 Eldridge et al 2002) Moreover multi-ple relationships between biocrusts and soil properties medi-ated by plants are expected to play a critical role in biocrustcommunity configuration even though they have been poorlystudied (Zhang et al 2016) Here vascular plant covertended to be higher in the embankments (39 ) than in theroadcuts (29 Table 3) However biocrust presence in theembankments was represented by only one species and it wasexclusively recorded at those sites with plant cover gt 30 (results not shown) It is also worth noting that although weonly estimated the cover of perennial plants we are awarethat annual plants can occupy almost the totality of peren-nial plant interspaces in the studied embankments but notin the roadcuts (personal observation) This suggests thatin embankments ndash habitats with less favorable soil condi-



tions for biocrusts as mentioned above ndash perennial and an-nual plant communities out-compete biocrusts by limitinghabitat space availability This hypothesis is somehow sup-ported by the fact that the roadcut with the lowest perennialplant cover registered a remarkably high cover of biocrusts(ca 9 results not shown) Notwithstanding our resultssuggest that complex bioticndashabiotic interactions operate inour road slopes Further work should explore the type (pos-itive vs negative) and magnitude of the effects that bothperennial and annual plants biocrusts and soil properties ex-ert on each other at very fine scales to better understand thenatural recovery process of these newly created habitats

Secondly we expected that biocrust communities at road-cuts and natural remnants would show differences in partic-ular ecological features such as gypsum and eutrophicationtolerance and thallus continuity Surprisingly communities atboth types of scenarios were rather similar in terms of gyp-sum and eutrophication tolerance However these findingssuggest that roadcuts and natural remnants present small dif-ferences in gypsum content and nutrient inputs or converselythat biocrust species can adapt well to varying environmen-tal conditions related to soil and air composition when suffi-cient microhabitat is available (ie low plant cover) Also aswe hypothesized biocrust communities had a slightly lowerCWM for thallus continuity in the roadcuts where less roughsurfaces can be found Our results are in accordance with thegenerally accepted scheme for biocrust succession where or-ganisms with smaller structural units (eg cyanobacteria andalgae) are the first to colonize new surfaces while more con-tinuous covers of lichens and mosses are found with time to-gether with increased soil microrelief (Belnap and Eldridge2003 Williams et al 2012)

Finally our results indicate that a particular combinationof topographic factors and soil properties was shared be-tween roadcuts and at least some of the adjacent natural rem-nants leading to a similar species composition It is wellknown that soil properties such as texture fertility and pH arestrong determinants of biocrust distribution patterns at the in-termediate and local scales (reviewed in Bowker et al 2016)Also the solar radiation load can shape biocrust communitiesthrough direct effects on biocrust organisms (eg ultravio-let radiation received) or indirectly by regulating soil mois-ture and vascular plant development (Bowker et al 2016)Accordingly we found that biocrust composition in roadcutsand natural remnants was at least in part driven by topog-raphy ie slope and heat load and several soil propertiesrelated to soil structure fertility and functioning ie stoni-ness EC soil K OC and acid phosphatase Indeed differ-ences in biocrust composition between roadcuts and naturalremnants were mainly due to soil and topographic character-istics but not to the type of environmental scenario per seThis is in agreement with Concostrina-Zubiri et al (2018)who reported that soil properties and topography explainedbiocrust diversity better than habitat structure (eg connec-tivity) and disturbance history (ie changes in habitat area)

in the studied landscape Nevertheless our results also sug-gest that intrinsic characteristics of roadcuts (eg soil ex-cavation generally higher slopes) embankments (eg soilcompacting) and natural remnants may exert an indirect ef-fect on biocrust composition mediated by the particular plantcommunity structure and composition associated with eachenvironmental scenario

43 New application of biocrusts as restoration tools indisturbed drylands recovery of road slope structureand function

The role of biocrusts as restoration tools in drylands has beengaining attention during the last 2 decades Biocrusts are nat-ural common components of drylands where high abioticstress conditions (ie high solar radiation low water and nu-trient inputs) typically combined with disturbance pressuresuch as grazing (Belnap 2003) make them one of the mostimportant elements for ecosystem structure and function incomparison to other systems dominated by vascular plantsDue to their resistance to harsh environmental conditions andlow resource requirements together with their relative easeof handling and interesting functional attributes (eg car-bon and nitrogen fixation soil stabilization soilndashwater dy-namic regulation) biocrusts are regarded as key organismsin dryland restoration research In fact higher biocrust coverhas been related to increased soil stability on road slopes inMediterranean grasslands contributing to the improvementof soil condition even more than vascular plants (Garciacutea-Palacios et al 2011) Therefore restoration strategies in dry-lands should begin to consider biocrusts as relevant commu-nities in the ecosystem recovery process as opposed to thetraditional ldquovascular-plants onlyrdquo approach Indeed it wouldbe interesting to test if the high vascular plant cover foundin road slopes (ca 30 ndash40 of mean cover Arenas et al2017a) is due to the amelioration of the initial soil conditionsby lichen and other biocrust types

So far it has been shown that biocrusts ndash including lichensndash can be grown artificially in the greenhouse rapidly (Do-herty et al 2015 Bowker and Antoninka 2016) and un-der field conditions as well (Xiao et al 2015) Moreovera few experiments have successfully applied biocrusts inthe field and continued growing and functioning have beenrecorded at least at the short term (Chiquoine et al 2016Condon and Pyke 2016 Antoninka et al 2017) Soil prop-erties such as organic matter content the inoculum type (iefield-collected vs greenhouse-cultured) the climatic similar-ity of collection and application zone and the initial speciescomposition of biocrusts to be applied are key points forthe success of biocrust re-establishment (Condon and Pike2016 Bowker and Antoninka 2016 Bowker et al 2017Antoninka et al 2017) Here we show that initial soil char-acteristics as given by road slope type are critical to sustain-ing relatively rich and diverse biocrusts in a road constructioncontext biocrust restoration efforts should be focused on ex-



cavated areas where bare soil and exposed bedrock dominate(eg roadcuts)

Recently the application of biocrust cyanobacteria inocu-lum (ie assisted recovery) has been identified as an effec-tive method for biocrust restoration in road slopes speed-ing up the recovery rate of biocrust cover and function toperiods shorter than 2 years (Chiquoine et al 2016) Forbiocrust lichens thalli translocation with the use of adhe-sives such as glue or simply water addition has also beenproposed as an effective measure to improve biocrust estab-lishment and assure functional recovery in disturbed gyp-sum soils (Ballesteros et al 2017) In this context com-mon andor relatively abundant species in road slopes suchas Enchylium spp or Gyalolechia spp can be consideredpromising species for active biocrust restoration Indeed itwould be interesting to collect specimens of these speciesat sites that will be converted to road slopes before the dis-turbance begins store them and then transplant them afterconstruction Conversely our findings suggest that naturalcolonization can also be regarded as an interesting restora-tion option although ecosystem recovery may take longer tooccur it has the advantage of increasing local diversity inthese human-made ecosystems as well as being highly cost-effective (Prach and Hobbs 2008)

5 Conclusions

Biocrust restoration offers an interesting opportunity to re-cover soil structure and function in disturbed drylands andprovides an alternative to traditional restoration techniquesusing vascular vegetation (Bowker 2007) This study evi-dences that lichen biocrusts can establish naturally on newlycreated habitats without any human assistance We also showthat topography and edaphic factors related to soil physi-cal characteristics (structure of roadcuts vs embankmentsstoniness) composition and functioning (as indicated byOC K EC and acid phosphatase values) play an importantrole in the configuration of new biocrust communities ontimescales of lt 20 years Actually we found that roadcutsand natural remnants with similar topography and soil prop-erties shared similar biocrust species composition Our find-ings thus suggest that given a certain combination of initialsoil properties and topographic factors biocrusts will likelydevelop successfully with no further actions needed Con-versely our results provide a number of promising speciesfor active biocrust restoration in Mediterranean road slopessince they are common (eg Enchylium spp) or can achieverelatively high cover (eg Gyalolechia spp) in such envi-ronmental scenarios Previous work has pointed out the roleof biocrusts in promoting soil stability in road slopes ofMediterranean grasslands (Garciacutea-Palacios et al 2011) Fu-ture research should evaluate the effect of lichens and otherbiocrust groups (eg cyanobacteria) on the improvement oftopsoil properties such as texture nutrient content and micro-

bial activity and assess biocrustndashvascular plant interactionsover time This would allow us to better quantify the contri-bution of biocrusts to ecosystem development in new land-scapes created after the construction of linear infrastructuresThis is particularly relevant in drylands due to their vulnera-bility to land-use change (Reynolds et al 2007)

Data availability Data are available from the Zenodo digitalrepository httpsdoiorg105281zenodo3237017 (Concostrina-Zubiri et al 2019)

Supplement The supplement related to this article is availableonline at httpsdoiorg105194we-19-39-2019-supplement

Author contributions LCZ JMA IM and AE conceived and de-signed the study LCZ and JMA conducted field work JMA andLCZ analyzed the data and LCZ JMA IM and AE wrote the pa-per

Competing interests The authors declare that they have no con-flict of interest

Acknowledgements L Concostrina-Zubiri and J M Arenaswere supported by the REMEDINAL-3 (S2013MAE-2719) ofthe Comunidad de Madrid Spain and by the European Union(Gypworld H2020-MSCA-RISE-2017-777803) We thank the twoanonymous reviewers for their comments which improved an ear-lier version of the paper

Financial support This research has been supported by theRampD Department of Obrascon Huarte Lain SA (OHL) theSpanish Ministry of Economy and Competitiveness (grant nosECONECT CDTI IDI-20120317 and ROOTS-CGL2015-66809-P)and the Madrid regional government (grant nos REMEDINAL-2S-2009AMB-1783 and REMEDINAL-3 S2013MAE-2719)

Review statement This paper was edited by Daniel Montesinosand reviewed by two anonymous referees

References

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Arenas J M Escudero A Mola I and Casado M A Road-sides an opportunity for biodiversity conservation Appl VegSci 20 527ndash537 httpsdoiorg101111avsc12328 2017a



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Arup U Soslashchting U and Froumldeacuten P A new taxonomyof the family Teloschistaceae Nordic J Bot 31 016ndash083httpsdoiorg101111j1756-1051201300062x 2013

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Bochet E Garciacutea-Fayos P Alborch B and Tormo J Soil wa-ter availability effects on seed germination account for speciessegregation in semiarid roadslopes Plant Soil 295 179ndash191httpsdoiorg101007s11104-007-9274-9 2007

Bowker M A Biological soil crust rehabilitation in theory andpractice an underexploited opportunity Restor Ecol 15 13ndash23 httpsdoiorg101111j1526-100X200600185x 2007

Bowker M A and Antoninka A J Rapid ex situ culture of N-fixing soil lichens and biocrusts is enhanced by complementarityPlant Soil 408 415ndash428 httpsdoiorg101007s11104-016-2929-7 2016

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Bowker M A Belnap J Buumldel B Sannier C Pietrasiak N El-dridge D J and Rivera-Aguilar V Controls on distribution pat-terns of biological soil crusts at micro-to global scales in Bio-logical soil crusts an organizing principle in drylands edited byWeber B Buumldel B and Belnap J Springer Cham Switzer-land 173ndash197 httpsdoiorg101007978-3-319-30214-0_162016

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Chamizo S Cantoacuten Y Laacutezaro R and Domingo F The role ofbiological soil crusts in soil moisture dynamics in two semiaridecosystems with contrasting soil textures J Hydrol 489 74ndash84httpsdoiorg101002hyp11493 2013

Chiquoine L P Abella S R and Bowker M A Rapidly restor-ing biological soil crusts and ecosystem functions in a severelydisturbed desert ecosystem Ecol Appl 26 1260ndash1272 2016

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Concostrina-Zubiri L Martiacutenez I and Escudero A Lichen-biocrust diversity in a fragmented dryland Fine scale factors arebetter predictors than landscape structure STOTEN 628 882ndash892 httpsdoiorg101016jscitotenv201802090 2018

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de Mendiburu F Package ldquoagricolaerdquo R Package Version 12-82017

Doherty K D Antoninka A J Bowker M A Ayuso S Vand Johnson N C A novel approach to cultivate biocrustsfor restoration and experimentation Ecol Restor 33 13ndash16httpsdoiorg103368er33113 2015

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Garciacutea-Palacios P Bowker M A Maestre F T Soliveres SValladares F Papadopoulos J and Escudero A Ecosystemdevelopment in roadside grasslands biotic control plantndashsoil in-teractions and dispersal limitations Ecol Appl 21 2806ndash2821httpsdoiorg10189011-02041 2011

Gypser S Veste M Fischer T and Lange P Formation ofsoil lichen crusts at reclaimed post-mining sites Lower LusatiaNorth-east Germany Graphis Scripta 27 3ndash14 2015

Gypser S Herppich W B Fischer T Lange P andVeste M Photosynthetic characteristics and their spatialvariance on biological soil crusts covering initial soils ofpost-mining sites in Lower Lusatia NE Germany Flora-



Morphology Distribution Funct Ecol Plant 220 103ndash116httpsdoiorg101016jflora201602012 2016

Hladun N and Llimona X Checklist of the lichens and licheni-colous fungi of the Iberian Peninsula and Balearic Islands avail-able at httpbotanicabioubeschecklistchecklisthtm (last ac-cess 1 December 2011) 2002ndash2007

Hui R Li X R Chen C Y Zhao X Jia R Liu L and WeiY Responses of photosynthetic properties and chloroplast ultra-structure of Bryum argenteum from a desert biological soil crustto elevated ultraviolet-B radiation Physiol Plant 147 489ndash501httpsdoiorg101111j1399-3054201201679x 2013

Jackson T A Study of the Ecology of Pioneer Lichens Mossesand Algae on Recent Hawaiian Lava Flows Pac Sci 25 22ndash32httpsdoiorg101256105 1971

Jimenez M D Ruiz-Capillas P Mola I Peacuterez-Corona ECasado M A and Balaguer L Soil development at the road-side a case study of a novel ecosystem Land Degrad Dev 24564ndash574 httpsdoiorg101002ldr1157 2011

Jimenez Aguilar A Huber-Sannwald E Belnap J Smart DR and Moreno J A Biological soil crusts exhibit a dynamicresponse to seasonal rain and release from grazing with im-plications for soil stability J Arid Environ 73 1158ndash1169httpsdoiorg101016jjaridenv200905009 2009

Lalley J S and Viles H A Recovery of lichen-dominated soilcrusts in a hyper-arid desert Biodivers Conserv 17 1ndash20httpsdoiorg101007s10531-007-9153-y 2008

Legendre P and Gallagher E D Ecologically meaningful trans-formations for ordination of species data Oecologia 129 271ndash280 httpsdoiorg101007s004420100716 2001

Luzuriaga A L Saacutenchez A M Maestre F T and EscuderoA Assemblage of a semi-arid annual plant community abi-otic and biotic filters act hierarchically PloS one 7 e41270httpsdoiorg101371journalpone0041270 2012

McCune B and Grace J B Analysis of Ecological CommunitiesMJM Software Design Gleneden Beach Oregon USA 2002

McCune B and Keon D Equations for potential annual directincident radiation and heat load J Veg Sci 13 603ndash606httpsdoiorg101111j1654-11032002tb02087x 2002

Mola I Jimeacutenez M D Loacutepez-Jimeacutenez N Casado M A andBalaguer L Roadside reclamation outside the revegetation sea-son management options under schedule pressure Restor Ecol19 83ndash92 httpsdoiorg101111j1526-100X200900547x2011

Niemi R Martikainen P J Silvola J Sonninen E WulffA and Holopainen T Responses of two Sphagnum mossspecies and Eriophorum vaginatum to enhanced UV-B in asummer of low UV intensity New Phytol 156 509ndash515httpsdoiorg101046j1469-8137200200532x 2002

Nimis P L and Martellos S ITALIC ndash The Information Systemon Italian Lichens Version 50 University of Trieste Dept ofBiology available at httpdryadesunitsititalic (last access 7January 2019 2016

Ninyerola M Pons X and Roure J Atlas Climaacutetico Digital de laPeniacutensula Ibeacuterica Metodologiacutea y aplicaciones en bioclimatologiacuteay geobotaacutenica Universidad Autoacutenoma de Barcelona BellaterraSpain 2005

Ochoa-Hueso R Hernandez R R Pueyo J J and Man-rique E Spatial distribution and physiology of biological soilcrusts from semi-arid central Spain are related to soil chem-

istry and shrub cover Soil Biol Biochem 43 1894ndash1901httpsdoiorg101016jsoilbio201105010 2011

Oksanen J Blanchet F G Friendly M Kindt R Legendre PMcGlinn D Minchin P R OrsquoHara R B Simpson G LSolymos P Henry M Stevens H Szoecs E and Wagner Hvegan Community ecology package R package version 25-22018

Otaacutelora M A Joslashrgensen P M and Wedin M A revised genericclassification of the jelly lichens Collemataceae Fungal Divers64 275ndash293 httpsdoiorg101007s13225-013-0266-1 2014

Pintado A Sancho L G Green T G A Blanquer J Mand Laacutezaro R Functional ecology of the biological soilcrust in semiarid SE Spain sun and shade populations ofDiploschistes diacapsis (Ach) Lumbsch Lichenologist 37425ndash432 httpsdoiorg101017S0024282905015021 2005

Prach K and Hobbs R J Spontaneous succession ver-sus technical reclamation in the restoration of disturbedsites Restor Ecol 16 363ndash366 httpsdoiorg101111j1526-100X200800412x 2008

Prieto M Aragoacuten G and Martiacutenez I The genus Cat-apyrenium s lat (Verrucariaceae) in the Iberian Penin-sula and the Balearic Islands Lichenologist 42 637ndash684httpsdoiorg101017S0024282910000319 2010a

Prieto M Martiacutenez I and Aragoacuten G The genus Placidiopsis inthe Iberian Peninsula and the Balearic Islands Mycotaxon 114463ndash472 httpsdoiorg105248114463 2010b

Prieto M Martiacutenez I Aragoacuten G Gueidan C and Lut-zoni F Molecular phylogeny of Heteroplacidium Placid-ium and related catapyrenioid genera (Verrucariaceaelichen-forming Ascomycota) Am J Bot 99 23ndash35httpsdoiorg103732ajb1100239 2012

Reynolds J F Smith D M S Lambin E F Turner IIB L Mortimore M Batterbury S P Downing T EDowlatabadi H Fernandez R J Herrick J E Huber-Sannwald E Jiang H Leemans R Lynam T Maestre FT Ayarza M and Walker B Global desertification build-ing a science for dryland development Science 316 847ndash851httpsdoiorg101126science1131634 2007

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Tormo J Brochet E and Garciacutea-Fayos P Restauracioacuten y reveg-etacioacuten de taludes de carreteras en ambientes mediterraacuteneossemiaacuteridos procesos edaacuteficos determinantes para el eacutexito Eco-sistemas 18 79ndash90 2009

Weber B Buumldel B and Belnap J (Eds) Biological Soil CrustsAn Organizing Principle in Drylands Springer Cham Switzer-land 2016a

Weber B Bowker M Zhang Y and Belnap J Natural Recoveryof Biological Soil Crusts After Disturbance in Biological SoilCrusts An Organizing Principle in Drylands edited by WeberB Buumldel B and Belnap J Springer Cham Switzerland 479ndash498 httpsdoiorg101007978-3-319-30214-0 2016b



Williams A J Buck B J and Beyene M A Biologi-cal soil crusts in the Mojave Desert USA micromorphol-ogy and pedogenesis Soil Sci Soc Am J 76 1685ndash1695httpsdoiorg102136sssaj20120021 2012

Xiao B Zhao Y Wang Q and Li C Development of artificialmoss-dominated biological soil crusts and their effects on runoffand soil water content in a semi-arid environment J Arid Envi-ron 117 75ndash83 httpsdoiorg101016jjaridenv2015020172015

Zhang Y Aradottir A L Serpe M and Boeken B Interac-tions of biological soil crusts with vascular plants in Biologi-cal Soil Crusts An Organizing Principle in Drylands edited byWeber B Buumldel B and Belnap J Springer Cham Switzerlandhttpsdoiorg101007978-3-319-30214-0_19 2016

Zuur A F Ieno E N and Smith G M (Eds) Principal com-ponent analysis and redundancy analysis in Analysing Eco-logical Data Springer New York New York USA 193ndash224httpsdoiorg101007978-0-387-45972-1_12 2007


Abstract

Introduction

Material and methods

Study area

Biocrust sampling and identification

Characterization of biocrust communities

Characterization of road slope topography soil properties and vascular plant communities

Data analyses

Results

Discussion

Natural recovery of biocrusts on new habitats

Biocrust structure and composition across environmental scenarios are mostly driven by topography and edaphic factors

New application of biocrusts as restoration tools in disturbed drylands recovery of road slope structure and function

Conclusions

Data availability

Supplement

Author contributions

Competing interests

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is less likely to occur due to a higher demand on soil re-sources and lower tolerance of water scarcity among others(Bowker 2007)

Biocrusts have been shown to recover naturally withoutassistance from mechanical disturbances such as grazingtrampling and vehicle driving and also from fire at varyingrecovery rates and following different community trajecto-ries depending on the disturbance type intensity and timing(Belnap and Eldridge 2003) However little is known aboutnatural recovery of biocrusts in newly formed and emer-gent habitats such as those generated after the constructionof linear infrastructures which include massive soil removalor the accumulation of exogenous soil material At the veryfine spatial scale (ie topsoil area lt 10 m2) several studieshave evaluated biocrust natural colonization and establish-ment after biocrust removal (ie scalping) Recovery ratesrange from less than 3 years for cyanobacteria commonlythe earliest fastest colonizers within biocrusts up to a fewdecades or almost a millennium for bryophytes and lichensthe typical components of more developed mature biocrusts(reviewed in Weber et al 2016b) Similarly to biocrust re-covery in secondary succession the colonization and estab-lishment of biocrusts largely depend on climate particularlyprecipitation amount and timing after disturbance and soilproperties such as soil stability and nutrient concentration(Weber et al 2016b)

Surprisingly to our knowledge there is only one studyfocusing entirely on the recovery of biocrust communitieson road slopes (Chiquoine et al 2016) Yet Chiquoineet al (2016) did not focus on natural colonization but onsuccessful establishment after applying biocrust inoculumamong other restoration treatments This is a bit strikingsince there is no baseline for comparison Therefore noprevious study has evaluated the unassisted recovery ofbiocrusts on road slopes and this limited knowledge onbiocrust recovery under natural conditions weakens manyprojects of ecological restoration of road slopes in drylands

In contrast many studies have highlighted the role of nat-ural colonization in the establishment of vascular vegeta-tion on road slopes (Bochet et al 2007 Mola et al 2011Arenas et al 2017a b) In Mediterranean drylands na-tive vascular plants can establish and develop well in roadslopes in the absence of human assistance when the slope isgentle (lt 45) (Bochet and Garciacutea-Fayos 2004) and suffi-cient propagule is available from the surroundings (Arenaset al 2017b) However species composition differs notablyfrom communities found in the natural surrounding areasmainly due to topography and modification of initial soilconditions derived from the process of road slope construc-tion (Bochet and Garciacutea-Fayos 2004 Arenas et al 2017a)Moreover within road slopes roadcuts and embankmentshave very different structural properties (eg soil removalvs soil application respectively) and environmental char-acteristics and as a result further differences can be foundbetween their respective plant communities at the compo-

sitional level (Arenas et al 2017a) For biocrusts we ex-pect to find processes of colonization and community as-sembly on road slopes similar to those that occur for vas-cular vegetation and therefore evidence the ecological in-terest of natural colonization as a useful biocrust restora-tion measure In particular we hypothesized that biocrustsestablish easily in the road slopes provided that biocrustsare common and abundant in the surroundings (ie inocu-lum availability) and because of their capacity to tolerateharsh environmental conditions typical for newly createdhabitats (eg very thin soil high radiation inputs) (Weberet al 2016b) Nevertheless we expect to find marked differ-ences in biocrust composition depending on road slope type(ie roadcut vs embankment) topography soil propertiesand vascular plant abundance since the diversity of these or-ganisms is highly sensitive to changes in (i) climate at thelocal and microscale given by topography eg sun vs shadeenvironments (Pintado et al 2005) (ii) soil physicochemicalproperties eg texture (Fischer and Subbotina 2014) nutri-ent content (Bowker et al 2006) and pH (Ochoa-Hueso etal 2011) and (iii) biotic interactions especially with vascu-lar plants eg biocrustndashplant facilitationndashcompetition pro-cesses (reviewed in Bowker et al 2016) In this study weaimed to assess the potential of lichen biocrusts to colonizeand prosper in pioneer habitats under natural conditions (iewith no artificial assistance) We focused only on lichens be-cause they are the most conspicuous rich and common com-ponents of biocrusts in Mediterranean grasslands and shrub-lands (Concostrina-Zubiri et al 2014) even in fragmentedlandscapes (Concostrina-Zubiri et al 2018)

Specifically we addressed the following questions (1) canlichen biocrusts establish on road slopes spontaneously Ifso (2) what species and functional attributes characterizethe newly formed communities Regarding the functionalattributes characterizing these communities we focused oneutrophication tolerance gypsum tolerance because ourbiocrust model occurs in this type of soil (Concostrina-Zubiriet al 2018) and thallus continuity to test the following hy-potheses (i) lichen biocrust communities in the road slopesare more tolerant to high nutrient levels (eg derived fromthe road traffic and the subsequent passive air fertilization)(ii) they present a higher tolerance ofaffinity to gypsum con-tent as expected in a less developed topsoil layer at roadslopes compared to natural remnants where soil carbon andother nutrients had higher levels (Arenas et al 2017a) and(iii) lichen biocrusts with a less continuous thallus are morelikely to colonize and prosper in road slopes characterizedby a more hostile microenvironment (3) What is the roleof habitat scenario type (eg road slopes vs natural areas)and other local factors (ie topography soil properties andvascular plant communities) in determining the structure andcomposition of lichen biocrusts By addressing these ques-tions we could identify the factors that determine the naturalcolonization of biocrust in road slopes and point out somerestoration measures to carry out in road slopes for promot-






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Data analyses

Results

Discussion




Conclusions

Data availability

Supplement


Competing interests

Acknowledgements

Financial support

Review statement

References

Unassisted establishment of biological soil crusts on dryland road … · 2020. 6. 4. · Laura...

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