PLANT MICROBE INTERACTIONS

Community Assembly of Biological Soil Crusts of DifferentSuccessional Stages in a Temperate Sand Ecosystem,as Assessed by Direct Determinationand Enrichment Techniques

Tanja Margrit Langhans & Christian Storm &

Angelika Schwabe

Received: 17 September 2008 /Accepted: 28 April 2009 /Published online: 30 May 2009# Springer Science + Business Media, LLC 2009

Abstract In temperate regions, biological soil crusts (BSCs:complex communities of cyanobacteria, eukaryotic algae,bryophytes, and lichens) are not well investigated regardingcommunity structure and diversity. Furthermore, studies onsuccession are rare. For that reason, the community assemblyof crusts representing two successional stages (initial, 5 yearsold; and stable, >20 years old) were analyzed in an inland sandecosystem in Germany in a plot-based approach (2×18 plots,each 20×20 cm). Two different methods were used to recordthe cyanobacteria and eukaryotic algae in these communitiescomprehensively: determination directly out of the soil andenrichment culture techniques. Additionally, lichens, bryo-phytes, and phanerogams were determined. We examine fourhypotheses: (1) A combination of direct determination andenrichment culture technique is necessary to detect cyanobac-teria and eukaryotic algae comprehensively. In total, 45species of cyanobacteria and eukaryotic algae were detectedin the study area with both techniques, including 26eukaryotic algae and 19 cyanobacteria species. With bothdetermination techniques, 22 identical taxa were detected (11eukaryotic algae and 11 cyanobacteria). Thirteen taxa wereonly found by direct determination, and ten taxa were onlyfound in enrichment cultures. Hence, the hypothesis issupported. Additionally, five lichen species (three genera),five bryophyte species (five genera), and 24 vascular plant

species occurred. (2) There is a clear difference between thefloristic structure of initial and stable crusts. The differentsuccessional stages are clearly separated by detrendedcorrespondence analysis, showing a distinct structure of thecommunity assembly in each stage. In the initial crusts,Klebsormidium flaccidum, Klebsormidium cf. klebsii, andStichococcus bacillaris were important indicator species,whereas the stable crusts are especially characterized byTortella inclinata. (3) The biodiversity of BSC taxa andvascular plant species increases from initial to stable BSCs.There are significantly higher genera and species numbers ofcyanobacteria and eukaryotic algae in initial BSCs. StableBSCs are characterized by significantly higher speciesnumbers of bryophytes and vascular plant species. The resultsshow that, in the investigated temperate region, the often-assumed increase of biodiversity in the course of succession isclearly taxa-dependent. Both successional stages of BSCs arediversity “hot spots” with about 29 species of all taxa per 20×20 cm plot. (4) Nitrogen and chlorophyll a concentrationsincrease in the course of succession. The chlorophyll acontent of the crusts (cyanobacteria, eukaryotic algae,bryophyte protonemata) is highly variable across the studiedsamples, with no significant differences between initial andstable BSCs; nor were ecologically significant differences insoil nutrient contents observed. According to our results, wecannot confirm this hypothesis; the age difference betweenour two stages is probably not big enough to show such anincrease.

Introduction

Especially in arid and semiarid regions but also inedaphically dry areas of the temperate zone, the lack of

Microb Ecol (2009) 58:394–407DOI 10.1007/s00248-009-9532-x

Electronic supplementary material The online version of this article(doi:10.1007/s00248-009-9532-x) contains supplementary material,which is available to authorized users.

T. M. Langhans : C. Storm :A. Schwabe (*)Department Biology, Vegetation Ecology,Darmstadt University of Technology,Schnittspahnstraße 4,64287 Darmstadt, Germanye-mail: Schwabe@bio.tu-darmstadt.de

water inhibits the development of a dense cover of vascularplant species. The soil surface is exposed to extremes intemperature and radiation. Nevertheless, in these harshenvironments, biological surface communities develop [23,37, 38]. They are usually dominated by cyanobacteria,eukaryotic algae, bryophytes, and lichens which aggregatewith soil particles. They have been referred to by multiplenames (see [33]), we use the term “biological soil crust”(BSC); for the components cyanobacteria, eukaryotic algae,and bryophyte protonema, we use the term “micro-crust.”

BSCs are highly diverse; the following numbers ofgenera have been found so far in BSCs worldwide [16]:Cyanobacteria, 35; eukaryotic algae, 68; cyanolichens, 13;chlorolichens, 69; and bryophytes, 62.

BSCs emerge from the activity of the biota in that soilparticles are bound together with polysaccharide exudatesand a matrix of fibers, thus forming a coherent layer [3, 18,55]. The physical stability of BSCs often results from thepresence of the cyanobacterium Microcoleus, which formsfilaments that are surrounded by extracellular sheaths. Themoving activity of the filaments through the wet soil andtherefore permanent renewal of the sheaths guarantees thestability of the soil [6]. This aggregation of the soil isobvious after disturbance or drying; cracks occur in theBSC, and the soil disintegrates into pieces [47], while soilwithout BSCs disintegrates into soil particles. Anothercommon genus of cyanobacteria in BSCs is Nostoc, whichoccurs in and especially on top of the crust. Nostoc coloniescan reach centimeters in diameter and are readily distin-guishable in the field. Additionally, Scytonema, Calothrix,and Gloeocapsa are frequently found. Eukaryotic algae arerepresented in BSCs by filamentous and coccoid species.Common genera of Chlorophyceae are Chlorella, Chloro-coccum, Coccomyxa, and Klebsormidium. Furthermore,Bacillariophyceae often occur (e.g., [51]).

BSCs are well studied in semiarid and arid environ-ments, e.g., in parts of the USA, Australia, Israel, and Asia,but only a few studies have been carried out in more humidclimates (e.g., [31, 51, 56]). Furthermore, plot-based dataare rare [40, 59]. The goal of this study is to investigate thediversity and community assembly of BSCs (includingvascular plant species) in a temperate region for twosuccessional stages with a plot-based approach. The studywas carried out in a threatened sand ecosystem (Koelerionglaucae vegetation complex) in the upper Rhine Valley inGermany.

A first aspect of our study is methodological. There arevarious methods with which to identify micro-crustorganisms. In several studies, the methods “direct deter-mination out of the soil” and “culturing” were combined(e.g., [35]), but the results were not individually presented,so that it is not possible to compare their relativeadvantages. Our hypothesis is that a combination of both

“direct determination and culturing” is needed to give acomprehensive account of the taxa the soil contains.Molecular analyses are also a common method, but theyare known to fail for otherwise conspicuous soil inhabitingcyanobacteria with thick sheaths, heterocysts, or certaingreen algae [17, 29].

BSCs are successional or permanent soil surface features(e.g., [13, 57]). Successional stages of crust communitiescan be distinguished [5]: Large filamentous cyanobacteriaoften colonize the substrate at first, followed by smallercyanobacteria and eukaryotic algae; mostly after soilstabilization, bryophytes and lichens are able to colonizethe soil. In general, base-rich sandy soils in arid regions areoften dominated by cyanobacteria, while eukaryotic algalcrusts mainly occur in more humid temperate regions withacidic soils (see [8]). Also, bryophyte-dominated crustswere recorded in more humid climates. Hardly any dataabout different crust stages in the course of succession areyet available and no data regarding micro- and macroscopicorganisms including vascular plant species. To allow for acomprehensive understanding of the successional develop-ment of BSCs, different taxonomical groups should bestudied, but many authors only have investigated thediversity of cyanobacteria and eukaryotic algae (e.g., [10])or of bryophytes and lichens (e.g., [24]). Vascular plantspecies have mostly not been included; however, underclimatically extreme conditions, they are absent.

In the present study, we distinguish two successionalstages: initial BSCs and stable BSCs (Fig. 1). Büdel et al.[17] described seven different crust types according to thedominant taxa cyanobacteria, lichens, and bryophytes alonga 2,000-km transect in SW Africa. The two types in ourtemperate system correspond to them [17] as follows:

– Initial crusts: “light cyanobacterial crust, initial (earlysuccessional stages)”

– Stable crusts: “cyanobacterial crust, well-established”

Our stable crusts partly are characterized by higherbryophyte dominance (see below), which is a transitiontype according to [17]: “crust with bryophytes, dominatedby mosses.” Crusts with higher dominance of cyano-/orgreen algal lichens are not present in our system, nor areliverwort crusts. Cyanobacteria, eukaryotic algae, andbryophytes are common in both crust types; lichens occurless and only with low cover.

Young, light-colored BSCs in our study area, whichwere approximately 5 years old in the year 2005 (developedafter a broad-scale disturbance by human impact), wereclassified as initial BSCs. Stable BSCs were older than20 years, having already been present in the early 1980s.Initial BSCs consisted of a 2-mm layer of organisms,whereas the layer in stable BSCs was approximately 3–5 mm thick.

Community Assembly of Biological Soil Crusts 395

Several studies of plant communities have indicated anincrease in biodiversity from the first to mid-successionalstages (e.g., [4, 28, 50, 68]). Diversity often then reverses,becoming lower in a terminal stage (e.g., [61]). Hence, thebiodiversity of taxa in BSCs should increase in the courseof early succession. According to the facilitation model ofConnell and Slatyer [19], the micro-crust should enhancethe probability of colonization for bryophytes and vascularplant species. Facilitation research is often restricted tointeractions of vascular plant species (reviewed in [15]).For BSCs, some studies exist (e.g., [12, 21]), but often,they deal with only a few species under laboratory

conditions (e.g., [49]). A field study by Breen andLévesque [14] along a High Arctic glacier forelandconcludes that BSCs facilitate vascular plant establishmentand growth in early and mid-succession.

The chlorophyll a content of BSCs is often used as acriterion for measuring the total density of crust organisms(e.g., [7, 66]). It varies from under 100 up to 900 mg m−2,depending on the crust composition [41, 44]. We includedchlorophyll a determinations to compare the two succes-sional stages. N2-fixing cyanobacteria constitute an impor-tant source of N input into the soil, and BSCs rich incyanobacteria are expected to have higher nitrogen contents

Figure 1 Crust types. aAn initial crust type (5 yearsold) dominated by cyanobacteriain the study area. The initialcrust in the center developedafter disturbance by humanimpact. In the foreground, T.ruraliformis moss-carpets withthe graminoids C. canescens andK. glauca. The area with theexperimental plots is fenced toprevent livestock disturbance. bClose-up of an initial crust type,dominated by cyanobacteria.Phanerogam vegetation withK. glauca, C. canescens,H. arenarium, and O. repens. cClose-up of an initial crust type,characterized by eukaryotic algae(dominated by Klebsormidiumand Zygogonium) and smallNostoc colonies. Vascularplant species are: S. conica, P.arenarium, S. acre, M. minima,and V. myuros. d Stable crusttype (>20 years old) in the studyarea (foreground); in the back-ground, T. ruraliformis mosscarpets and graminoid-dominatedKoelerion glaucae. e Close-up ofthe stable crust type, dominatedby cyanobacteria (especiallyMicrocoleus, Nostoc). The 20×20 cm plot in the center ismarked with two different tagtypes (to locate the orientation).f Close-up of the stable crusttype with the cyanolichenCatapyrenium after a dry period.g Close-up of the stable crusttype with two Nostoc communecolonies (center), T. ruraliformis(upper part) and the indicatorspecies for stable crusts in oursystem: T. inclinata (left side);after a wet period

396 T. M. Langhans et al.

than BSCs with scarce abundance of cyanobacteria (e.g.,[34, 36]). Furthermore, it can be hypothesized that thenitrogen contents of the BSCs increase with the course ofsuccession.

To sum up, the objective was to test the followinghypotheses:

1. A combination of direct determination and enrichmentculture technique is necessary to detect cyanobacteriaand eukaryotic algae comprehensively.

2. There is a clear difference between the floristicstructures of initial and stable crusts.

3. As generally supposed for early successional processes,the biodiversity of BSC taxa and vascular plant speciesincreases from initial to stable BSCs.

4. Likewise, nitrogen and chlorophyll a concentrationsincrease.

Materials and Methods

Study Area

The study area (“Ehemaliger August-Euler-Flugplatz vonDarmstadt”) is situated in the sand ecosystems of Darmstadtin the northern upper Rhine valley in south Hesse,Germany (district Darmstadt; 8°35′ E/49°51′ N). The soilsubstrate in this area is drifted sand which had been blownout from calcareous Rhine deposits during late glacial andpost-glacial periods [1]; the study area was in the glacierfree corridor. The soil type at the BSC plots is calcaricArenosol with silt + clay content <10% and pH in thetopsoil ranging from 7.1 to 7.7 [31] (determined in0.01 mol l−1 CaCl2). The mean temperature (±SE) is ca.10.8±0.6°C, the annual precipitation is 608±124 mm a−1,and the annual duration of sunshine is 1,686±151 h (1991–2004, Frankfurt Airport, Deutscher Wetterdienst; www.dwd.de/de/FundE/Klima/KLIS/daten/online/nat/index/index.htm). The study area belongs to the biogeographicalcentral European transition zone between subatlantic,submediterranean, and subcontinental influence, as isshown by the occurrence of vascular plant species withdifferent distribution areas (e.g., Koeleria glauca—(sub)continental, Corynephorus canescens—suboceanic, andSilene otites—submediterranean distribution).

The area has been subject to severe human impact forcenturies (at least 500 years), which guaranteed theexistence of pioneer plant communities and open grass-lands. Extensive military use continued until the lastcentury. Aerial photographs from 1934 give evidence oflarge areas of open sand.

The vegetation mainly consists of low-productivitypioneer plant communities (Koelerion glaucae vegetation

complex). The eastern parts of the study area represent asmall-scale mosaic which is dominated by therophytes andthe bryophyte species Tortula ruraliformis. The opencanopy of these stands allows for the occurrence ofBSCs [48].

The surfaces of these BSCs were rugose with a lowsurface roughness of about 1 cm. Initial crusts were light-colored, young crusts (5 years old), with a thin layer oforganisms (approximately 2 mm). Stable crusts werepinnacled older crusts (>20 years old), with always a thicklayer of organisms (approximately 3–5 mm). In 2005, themean total crust cover (±SE) of initial BSCs per plot was65.9±5.2%, including a mean bryophyte cover (±SE) of28.3±5.5% and a mean lichen cover of<1%. The meancover of vascular plants was 7%. Stable BSCs showed acrust cover of 69.5±5.2% including a higher bryophytecover of 37.7±6.4%. The covers of lichens and vascularplants were similar in initial and stable crusts.

Field Sampling for Direct Determination and Culturing

Eighteen random samples of initial and 18 of stable crustswere taken in August 2005 (initial BSCs) and September2002 (stable BSCs). The 2 years were similar in referenceto temperature (mean temperature 2002, 11.2°C; 2005,11.0°C) and precipitation (precipitation in the month beforeremoval 2002, 54 mm; 2005, 47 mm). The sampling wascarried out in a plot-based approach with an aluminumframe (20×20 cm) which was pushed 1.5 cm deep into thesoil. The sample was then cut out of the soil by a plate.Afterwards, the samples were oven dried for 60 h at 35°Cand stored (1–3 years) in a dark and dry room untildetermination. Before removal of the BSCs, the number ofvascular plant species on each plot was recorded.

Direct Determination

The determinations were made directly out of the crust after1 h rewetting (four subsamples 2×2 cm per 20×20 cmplot). For determination, a Zeiss Axiostar Plus was used.For details on size, minimally ten individuals of each of thedifferent species were measured. The organisms wereidentified according to Geitler [30], Ettl and Gärtner [25],and Komárek and Anagnostidis [42, 43]. Bryophytes andlichens were determined according to Frahm and Frey [27]and Wirth [69].

Enrichment Cultures

We applied the culturing conditions described by Ettl andGärtner [25] (daylight, 20°C). For culturing eukaryoticalgae, Bold's Basal Medium (BBM) [11] and, for cyano-bacteria, BG 11 [58] were used. Enrichment cultures of the

Community Assembly of Biological Soil Crusts 397

soil samples were raised by placing 1 g soil in 20 ml BBM(two replicates) or BG 11 (two replicates) media containedin 100-ml Erlenmeyer flasks. Additionally, solid mediawere made with 1% agar and put into Petri dishes (tworeplicates per medium). One gram substrate was added ontothe surface. Afterwards, the samples were exposed at roomtemperature under an irradiance of approximately 500μmolphotons m−2 s−1 and a light–dark regime of 10:14 h. Themedium was changed when the first was exhausted. Taxawere determined after 3–6 months.

Nutrient Contents

Nutrient contents of BSCs were analyzed in August 2005(ninitial=18; nstable=18). Two individual samples were takenfrom a depth of 3 cm with a soil sample ring (53 mm indiameter; Eijkelkamp, Agrisearch Product 07.01), bulked togive one composite sample and kept cool to preventmicrobial nitrogen mineralization. Within 24 h, the sampleswere sieved (2 mm) and frozen (−18°C) until extraction.According to VDLUFA [67], plant-available nitrogen andammonium were measured in calcium chloride extracts(0.0125 mol l−1) and phosphate in calcium acetate/calciumlactate extracts. Analyses were carried out photometricallywith a Skalar SAN. All results regarding soil data refer todry soil (24 h, 105°C).

After drying (70°C) and grinding of another aliquot ofthe composite samples, total nitrogen content was deter-mined by means of a N-analyser (Carlo Erba 1400).Accuracy was ascertained by the use of certified material(soil standard 5 with certified value 0.021% N, our value0.022% N (n=5); soil standard 2 with certified value0.064% N and our value 0.063% N (n=5); HEKAtechGermany).

Chlorophyll a Determination

Thirty plots of initial and 30 of stable crusts weresampled in August 2005. Sterile Falcons were pressed1 cm deep into the substrate. For each plot, threesubsamples were taken, afterwards closed and stored at−18°C until extraction. For extraction, the samples werethawed, the macroscopic moss plants (but not theirprotonemata) were removed, and afterwards the subsam-ples were bulked and mixed. Approximately 1 g of thesoil substrate (including the micro-crust) was used fordetermination. Chlorophyll a was extracted in 10 ml99.5% dimethyl sulfoxide for 90 min at 65°C according tothe method of Ronen and Galun [60]. Twenty-five milli-grams CaCO3 was added to avoid acidification and theresulting pheophytinization of chlorophyll. The chloro-phyll content was calculated [2] after spectrophotometrywith a Spectronic Genesys 5.

Data Analyses

To determine differences between initial and stable BSCs, ttests were used in case of approximate normal distribution(in case of heterogenous variances, as indicated by Levene'stest, Welsh's t test was applied): bryophyte species,eukaryotic algae species in cultures, cyanobacteria speciesin cultures, eukaryotic algae species in combined data,genera of cyanobacteria in soil, bryophyte genera, eukary-otic algae genera in cultures, eukaryotic algae genera incombined data, phosphate and mineral N (ammonium+nitrate) contents.

U tests were used for non-normal data: eukaryotic algaeand cyanobacteria species in soil, lichen species, cyanobac-teria species in combined data, eukaryotic algae genera insoil, lichen genera, cyanobacteria genera in cultures,cyanobacteria genera in combined data, vascular plantspecies, total species numbers, and chlorophyll a, nitrate,ammonium as well as total N contents.

The taxa composition of BSCs (cyanobacteria andcryptogams) was analyzed by means of detrended corre-spondence analysis (DCA) using PC-ORD 5. The analysiswas run on presence/absence data with downweighting ofrare species and rescaling; the number of segments was 26.

Results

Direct Determination Out of the Rewetted Soil (Bryophytesand Lichens Included)

In initial BSCs, we found 14 genera of eukaryotic algae(including five genera of Pennales), nine genera ofcyanobacteria, three genera of lichens (two genera chloro-lichens, one genus cyanolichens), and two genera ofbryophytes (Table 1); in stable BSCs, we found 11 generaof eukaryotic algae (including two genera of Pennales),nine genera of cyanobacteria, three genera of lichens (twogenera chlorolichens, one genus cyanolichen), and fivegenera of bryophytes (Table 1).

Mean genera numbers of eukaryotic algae do not show asignificant difference between initial and stable BSCs(Fig. 2a; p=0.6442). In contrast, the mean genera numbersof cyanobacteria were significantly higher in stable than ininitial BSCs (p=0.0152). Furthermore, the mean generanumbers of bryophytes were higher in stable (3.1±0.1) thanin initial (1.5±0.2) BSCs (p<0.0001). Lichen generaoccurred in small numbers (initial, 0.9±0.2; stable, 0.6±0.1) and exhibited no significant differences between thecrust types (p=0.2040).

In initial BSCs, 17 species of eukaryotic algae, 15species of cyanobacteria, four species of lichens (twospecies of chlorolichens and two species of cyanolichens),

398 T. M. Langhans et al.

Table 1 Presence of the species detected by determination out of the rewetted soil (direct) and after culturing (culture) in percent

Initial BSCs direct Stable BSCs direct Initial BSCs culture Stable BSCs culture

A Bracteacoccus cf. minor 22 39 22 83

A cf. Chlorosarcinopsis sp. – – 6 –

A Chlamydomonas sp. 11 – 6 –

A Chlamydomonas cf. reinhardtii – – 11 –

A Chlorella cf. vulgaris – – – 33

A Chloridella/Pleurochloris sp. 44 78 83 89

A Chlorococcum cf. infusionum 89 39 100 100

A Coccomyxa cf. confluens – – 11 33

A cf. Cylindrocystis sp. 11 61 – –

A Cylindrocystis cf. brebissonii – – 56 –

A Cylindrocystis cf. crassa – – 6 –

A Elliptochloris cf. subsphaerica 11 22 22 89

A Gloeocystis cf. vesiculosa 28 6 11 –

A Klebsormidium cf. crenulatum 17 – 44 –

A Klebsormidium cf. dissectum – – 56 –

A Klebsormidium flaccidum 50 11 100 –

A Klebsormidium cf. klebsii 28 11 89 –

A Scenedesmus acutus – 6 39 –

A Stichococcus bacillaris – – 94 6

A Zygogonium ericetorum 100 100 22 –

A Pennales 01 (cf. Navicula) 28 56 – –

A Pennales 02 (cf. Hantzschia) 17 28 – –

A Pennales 03 (cf. Cymbella) 11 – – –

A Pennales 04 (cf. Pinnularia) 11 – – –

A Pennales 05 (cf. Navicula) 17 56 – –

A Pennales 06 (cf. Eunotia) 11 – – –

C Chroococcus pallidus 56 50 50 28

C Gloeocapsa compacta 11 94 50 6

C Lyngbya sp. 22 6 61 –

C Microcoleus vaginatus 94 100 – 11

C Microcoleus cf. paludosus 17 56 – –

C Nostoc cf. calicola – – 17 –

C Nostoc commune 78 94 100 28

C Nostoc cf. minutum 17 33 78 11

C Nostoc microscopicum 83 94 72 72

C Oscillatoria sp. 01 33 – – –

C Oscillatoria sp. 02 72 89 78 44

C Oscillatoria sp. 03 44 50 6 –

C Oscillatoria sp. 04 94 50 – –

C Oscillatoria sp. 05 – 11 – –

C Phormidium sp. 44 83 – –

C Phormidium cf. autumnale – 6 22 6

C cf. Schizothrix friesii – – 11 –

C Synechococcus cf. sciophilus 89 78 – –

C Tolypothrix fasciculare 78 72 100 61

L Cetraria aculeata 39 6

L Cladonia furcata agg. – 28

L Cladonia pyxidata agg. 17 33

L Collema crispum 17 –

Community Assembly of Biological Soil Crusts 399

and two species of bryophytes were determined (Table 1).In stable BSCs, 13 species of eukaryotic algae, 16 speciesof cyanobacteria, four species of lichens (three chloroli-chens and one cyanolichen), and five species of bryophyteswere determined (Table 1). The mean species number ofeukaryotic algae (Fig. 2b) showed no significant differencebetween initial and stable BSCs (p=0.7699), while themean species number of cyanobacteria (Fig. 2b) revealed asignificant difference between initial and stable crusts (p=0.0311). The mean species numbers of lichens were similarin initial and stable BSCs (p=0.5025). In contrast, the meanspecies numbers of bryophytes revealed a significantdifference. Stable BSCs presented higher mean speciesnumbers than initial BSCs (p<0.0001).

Determination by Means of Cultivation

In assaying the different cultures, we determined ininitial BSCs 13 genera of eukaryotic algae and sevengenera of cyanobacteria (Table 1). Stable BSCs consistedof eight genera of eukaryotic algae and seven genera ofcyanobacteria (Table 1). These differences between initialand stable BSCs were significant in both cases. The meangenera number of eukaryotic algae was 1.4-fold higher ininitial than in stable crusts (p=0.0059, Fig. 2a). Forcyanobacteria, the mean genera numbers in initial crustswere 2.1-fold higher than in stable ones (p<0.0001,Fig. 2a).

In total, we could determine 26 eukaryotic algaespecies and 13 species of cyanobacteria. The highestspecies diversity was found in cultures from initial crusts(18 species of eukaryotic algae and 12 species ofcyanobacteria). Out of stable BSCs, seven species ofeukaryotic algae and nine species of cyanobacteria couldbe cultivated. Significant differences between the meanspecies numbers of eukaryotic algae and cyanobacteria(Fig. 2b) of initial and stable BSCs occurred (p<0.0001;p<0.0001). The highest species numbers of eukaryoticalgae as well as cyanobacteria were recorded from culturesof initial BSCs. The mean species numbers of eukaryotic

Table 1 (continued)

Initial BSCs direct Stable BSCs direct Initial BSCs culture Stable BSCs culture

L Collema tenax 28 22

B Brachythecium albicans – 6

B Bryum argenteum – 50

B Hypnum cupressiforme var. lacunosum 50 50

B Tortella inclinata – 100

B Tortula ruraliformis 100 100

Total sample area for each crust type was 0.72 m2 (n=18)

A alga, C cyanobacterium, L lichen, B bryophyte

0

1

2

3

4

5

6

7

8

9

initi

al_s

oil

stab

le_s

oil

initi

al_c

ultu

re

stab

le_c

ultu

re

initi

al_c

ombi

ned

stab

le_c

ombi

ned

mea

ng

ener

an

um

ber

s[+

/-S

E]

algae

cyanobacteria

a aAA

aa

A

Ba

bA

B

0

2

4

6

8

10

12

14

initi

al_

soil

sta

ble

_so

il

initi

al_

cultu

re

stab

le_

cultu

re

initi

al_

com

bin

ed

sta

ble

_co

mbi

ned

mea

nsp

ecie

snu

mbe

rs[+

/-S

E]

algae

cyanobacteriaa

b

AB

a a

A

Ba

bA

B

A

B

Figure 2 a Mean genera numbers of eukaryotic algae andcyanobacteria [±SE] for initial and stable BSCs. Soil directdeterminations; culture enrichment cultures; combined both methodscombined. Different letters indicate significant differences (p<0.05)(minuscule differences between the mean species numbers ofeukaryotic algae; capital letters differences between mean speciesnumbers of cyanobacteria). b Mean species numbers of eukaryoticalgae and cyanobacteria [±SE] for initial and stable BSCs. Soil directdeterminations; culture enrichment cultures; combined both methodscombined. Different letters indicate significant differences (p<0.05;minuscule differences between the mean species numbers ofeukaryotic algae; capital letters differences between mean speciesnumbers of cyanobacteria)

400 T. M. Langhans et al.

algae were significantly higher than those of cyanobacteriain cultures of both initial (p=0.0014) and stable (p=0.0002)BSCs.

Combined Data (Direct Determination and EnrichmentCultures)

Genera and Species

In total, 45 species were detected in the study area withboth techniques; including 26 eukaryotic algae species (18genera), 19 cyanobacteria species (10 genera), additionallyfive lichen species (three genera), and five bryophytespecies (five genera) occurred.

The mean genera numbers of eukaryotic algae andcyanobacteria in initial and stable BSCs are shown inFig. 2a. In initial BSCs, the mean genera numbers ofeukaryotic algae were similar to those in stable BSCs (p=0.6921), and the mean genera numbers of cyanobacteriaalso revealed no differences between initial and stableBSCs (p=0.2862).

A t test revealed significantly more eukaryotic algaespecies (Fig. 2b) in initial than in stable BSCs (p=0.0021),and the same is true for cyanobacteria species (p=0.0486).Mean species numbers of lichens and bryophytes wereobtained only by direct determination (for results, seeabove).

With the combination of both techniques, we detected ininitial BSCs ten eukaryotic algae species and nine cyano-bacteria, in stable BSCs four eukaryotic algae species andeight cyanobacteria. In cultures, eight species of eukaryoticalgae and two species of cyanobacteria were exclusivelyfound, whereas seven eukaryotic algae and six cyanobac-teria species were only determined directly in the soil.Species of Pennales were exclusively found with directdetermination. When initial and stable BSCs were com-pared, several indicator species were found for initial crusts(i.e., found in initial but not in stable crusts); three speciesof Pennales and one Oscillatoria were detected by directdetermination, and seven species were detected in culturesfrom initial BSCs (cf. Chlorosarcinopsis, Chlamydomonas

cf. reinhardtii, two Cylindrocystis, one Klebsormidium, oneNostoc, and cf. Schizothrix). Only two indicator specieswere present in stable crusts (Oscillatoria sp., found bydirect determination, and Chlorella cf. vulgaris, found afterculturing).

Ordination

Figure 3a shows the DCA of all determined crustorganisms (both methods combined). The different crusttypes are clearly separated along the first axis: on the leftside initial BSCs, on the right stable BSCs. Therefore, axis1 represents the successional gradient. The short gradientlength (half change) shows that many taxa occur in bothcrust types.

In Fig. 3b, some species are shown with differentpositions in the successional stages. Klebsormidiumflaccidum, Klebsormidium cf. klebsii, and Stichococcusbacillaris were mostly determined on initial BSCs;whereas Tortella inclinata was only detected in stableBSCs. These are the most important indicator species forinitial and stable crusts.

Vascular Plants

Mean species numbers of vascular plants show significantdifferences between initial and stable BSCs (p=0.0183): oninitial BSCs, 5.6±0.46 (mean ± SE) species were found,whereas on stable BSCs, 7.25±0.28 species were presenton the 20×20 cm plots. The species found only in initialBSCs was Poa bulbosa. In contrast, Conyza canadensis,Koeleria macrantha, Rumex acetosella, and Veronica vernawere recorded only on plots with stable BSCs. Thefollowing species were found in both crust types: Arenariaserpyllifolia, Bromus tectorum, Cerastium semidecandrum,C. canescens, Erodium cicutarium, Erophila verna, Eu-phorbia cyparissias, Helichrysum arenarium, K. glauca,Medicago minima, Mysosotis stricta, Phleum arenarium,Salsola kali ssp. tragus, Saxifraga tridactylites, Sedumacre, Setaria viridis, Silene conica, Veronica praecox, andVulpia myuros.

Overall Results

When the data from field determination and cultivation arecombined, there is a significant decrease in the meanspecies numbers of cyanobacteria and eukaryotic algae,whereas the mean species numbers of vascular plants andbryophytes significantly increased in the course of succes-sion (Fig. 4). Only the mean species numbers of lichens didnot show a significant difference between initial and stableBSCs. The total species numbers of cyanobacteria andcryptogams on a 20×20 cm plot for initial BSCs was 24.1±

Table 2 Mean nutrient contents [±SE] of 18 initial and 18 stableBSCs in 2005 (0–3 cm soil depth)

PO43−–P

(mg kg−1)NO3

−–N(mg kg−1)

NH4+–N

(mg kg−1)Total N (%)

InitialBSCs

9.30±0.66 5.10±0.49 3.51±0.29 a 0.0536±0.002

StableBSCs

9.82±1.03 6.08±0.68 2.55±0.11 b 0.0539±0.003

Different letters indicate significant differences between initial andstable BSCs.

Community Assembly of Biological Soil Crusts 401

0.8 and for stable BSCs 21.9±0.6, which is not a significantdifference (p=0.0596). When vascular plant species wereincluded, the total species number was 29.4±0.8 for initialand 29.2±0.8 for stable BSCs (p=0.8862).

Soil Nutrient Contents

Initial and stable BSCs (Table 2) show no significantdifferences in phosphate (p=0.6396) and nitrate-N contents(p=0.3589) nor in the total N content (p=0.8993). Asignificant difference occurs for ammonium N (p=0.0177),which was lower in stable compared to initial BSCs, but ifnitrate N and ammonium N are summed up (total mineralN), initial and stable BSCs are not significantly differentagain (p=0.9856).

Chlorophyll a Content

There are no significant differences (Table 3) betweeninitial and stable BSCs (p=0.1602). Additionally, there is ahigh variability in the chlorophyll a content within the crusttypes. In initial BSCs, the lowest value was 5.7 μg g−1

(28.4 mg m−2) and the highest 59.0 μg g−1 (294.8 mg m−2).In stable crusts, the differences were smaller (lowest2.3μg g−1, 11.3 mg m−2; highest 26.8 μg g−1, 134.2 mg m−2).

Discussion

When these data were compared to the list of generareported from soil crusts in Europe [16], we found ten out

-20

0

20 60 100 140

40

80

120

Axis 1

Axis

2

-20

0

20 60 100 140

40

80

120

Axis 1

Axis

2

-20

0

20 60 100 140

40

80

120

Axis1

Axis

2

-20

0

20 60 100 140

40

80

120

Axis 1

Axis

2

a b

c d

-20

0

20 60 100 140

40

80

120

Axis 1

Axis

2

a

b

Figure 3 a Occurrence of allcrust organisms (combinedpresence/absence data of directdetermination and enrichmentcultures). Open symbols initialBSCs; filled symbols stableBSCs. Axis 1 eigenvalue 0.225,gradient length 1.49; Axis 2eigenvalue 0.076, gradientlength 1.27; Axis 3 eigenvalue0.051, gradient length 1.25. bOrdination of (a) S. bacillaris,(b) K. cf. klebsii, (c) K. flacci-dum, (d) T. inclinata; smallsymbol: species not present(same data as Fig. 2a)

402 T. M. Langhans et al.

of the 18 genera of cyanobacteria and 15 out of the 26genera of eukaryotic algae in our study area. Bryophytesand especially lichens are represented with lower diversitythan cyanobacteria and eukaryotic algae. Four out of the 14genera of bryophytes were detected in our study area. Onlyfour out of the 34 lichen genera were detected in our studyarea, three out of 29 chlorolichens, and one out of fivecyanolichens.

Most studies on BSCs have been restricted to specifictaxonomic groups (Table 4). The biodiversity in ourtemperate sand ecosystem is no lower than those in hotarid, semiarid, or arctic areas (Table 4; mostly in thesestudies, no information about the sampled areas isprovided). Partly taxonomic diversity of cyanobacteria ishigher in winter rain zones of SWAfrica (58 species in thehuge transect of Büdel et al. [17]), but if only one studyarea is compared to our system, the results are verysimilar.

Many of the species occurring in our area, especiallyfrequent ones, are widespread soil species with broadecological amplitudes (e.g., K. flaccidum and Microcoleusvaginatus) and are common worldwide. Nostoc, Gloeo-capsa, Chlorococcum, and Stichococcus species were alsodetected in BSCs from arid regions (e.g., [45]). M.vaginatus and Microcoleus paludosus are common cyano-

bacteria and were often determined in initial and stableBSCs; they are also known from crusts in arid zones(compare [8, 59]). The species composition of cyanobac-teria and eukaryotic algae found in our base-rich systemdiffers from the species composition reported from acidareas in central Europe (compare [51–53]); in particular,our system is richer in cyanobacteria.

Bryophyte species like T. ruraliformis are adapted todrought stress and therefore occur frequently in crusts.Tortula was recorded by many authors and is a commongenus (e.g., [20, 59]). But also, bryophyte species thatnormally live in less stressful environments were present,probably due to the seasonally varying quantity ofprecipitation.

Hypothesis 1

The comparison of the taxa detected by direct determina-tion and after cultivation clearly supports hypothesis 1: Acomprehensive account of the biological diversity of themicro-crust cannot be achieved by one method only. Directdetermination especially underestimated eukaryotic algae(Pennales excluded), and the culturing method did notdetect all cyanobacteria.

On the one hand, an advantage of the cultivation methodis that it can amplify some taxa which occur withfrequencies too low to be detected by direct determination.Moreover, the organisms which are determined directly outof the soil represent the community structure at thesampling date, whereas the cultured organisms also showthe “hidden diversity” of the community which wouldpotentially develop under suitable abiotic and bioticconditions in the course of the year. The resistant stagesof eukaryotic algae are present in the field, but mostly, they

Table 3 Mean chlorophyll a contents [±SE] of 30 initial and 30 stableBSCs in 2005

Chl a (μg g−1) Chl a (mg m−2)

Initial BSCs 22.8±2.6 114.0±12.9

Stable BSCs 16.6±1.4 82.9±6.8

0

2

4

6

8

10

12

14

initial BSCs stable BSCs

mea

n s

pec

ies

nu

mb

ers

[+/-

SE

]

algae cyanobacteria lichens bryophytes vasc. plant sp.

*

n.s.

***

**

*

Figure 4 Mean species numb-ers of eukaryotic algae, cyano-bacteria, bryophytes, lichens,and vascular plant species [±SE]for the combined data (directdetermination and enrichmentcultures). n.s. not significant; *p<0.05; **p<0.01; ***p<0.0001

Community Assembly of Biological Soil Crusts 403

cannot be identified by direct determination. They developin culture or in other seasons and therefore are “hidden” indry conditions. The importance of seasonality in theorganisms' occurrence was worked out by Hahn andKusserow [32], who studied cultures of crust samples fromthe Sahel of West Africa.

On the other hand, not every organism can be culturedeasily, especially the cyanobacteria. The difficulties pre-venting correct identification are isolation of single cells orthe lack of life-cycle information.

Several other authors used combined determinationmethods (e.g., [17]). Hawkes and Flechtner [35] couldpresent only two cultured species of cyanobacteria, while14 species were observed directly. As already mentioned,molecular analyses fail for cyanobacteria with thicksheaths, heterocysts, or certain green algae [17, 29].

Hypothesis 2

The structure of the community assembly differs clearly,which is shown by the DCA. Initial crusts are characterizedby different Klebsormidium species, which was (e.g.) alsoshown for post-mining Central Europe [31].

Both initial and stable BSCs contained bryophytes andlichens in our study area; initial crusts had only earlysuccessional taxa like T. ruraliformis and the cyanolichenCollema, while stable BSCs also are characterized bybryophytes and chlorolichens from later stages (Brachythe-cium, Bryum, Cladonia).

Hypothesis 3

The change of biodiversity in the course of succession frominitial to stable BSCs is clearly taxa-dependent. We detectedan increase of bryophytes and vascular plant species numbersbut a significant decrease for cyanobacteria and eukaryoticalgae. Initial crusts presented the highest diversity ofeukaryotic algae. The presence of nitrogen-fixing cyanobac-teria with notable abundances was not restricted to stableBSCs; in contrast, we were able to cultivate Nostoc andTolypothrix from almost all initial crusts.

BSCs are highly diverse in the investigated successionalstages, when the species numbers of vascular plants,cryptogams, and cyanobacteria are summed up. Whenvascular plant species and cryptogam/cyanobacteria speciesare compared, the latter are more diverse than vascularplant species. The pioneer vascular plant vegetation of aKoelerion glaucae complex is more diverse than thevascular plant species found in BSCs. Species numbersranged from 29 to 44 per 25 m2 in 2005 [Schwabe, n.p.];nevertheless, many species of the Koelerion glaucaecomplex were present in BSCs. Common garden experi-ments carried out by Langhans et al. [47] with initial andstable BSCs revealed inhibition by stable BSCs for severalspecies (Alyssum montanum ssp. gmelinii, Helianthemumnummularium, and S. otites); therefore, some vascular plantspecies may actually be inhibited by stable crusts. For thevascular plant species which were present in this study,there are no data as yet.

Table 4 Taxa diversity in site-specific studies on BSCs

Citation State Total taxa C A L B Size per plot Sampled area

Kaštovská et al., 2005 [40] Svalbard 73 48 25 – – 10 cm2 24 plots

Shubert and Starks, 1980 [63] AZ, NM, ND, USA 11 5 6 – – n.s. 17 sites

Shields and Drouet, 1962 [62] NV, USA 16 12 4 – – n.s. n.s.

Johansen et al., 1984 [39] UT, USA 57 15 33 5 4 n.s. 32 samples

Hawkes and Flechtner, 2002 [35] FL, USA 35a – – – – n.s. 150 samples

Flechtner et al., 1998 [26] Mexico 67 18 49 – – n.s. 10 sites à 10 samples

Rivera-Aguilar et al., 2006 [59] Mexico 34 7 – 8 19 225 cm2 87 sites

Bhatnagar et al., 2008 [10] India 83a – – – – 900 cm2 27 sites, 51 samples

Lange et al., 1992 [45] Israel 7 4 2 1 – n.s. n.s.

Cabała and Rahmonov, 2004 [18] Poland 11 6 5 – – 61 cm2 17 sites

Langhans et al., this study Germany 62 19 32 6 5 400 cm2 36 plots

Lukešová, 2001 [50] CZ, Germany 122a – – – – n.s. 16 sites

Malam et al., 1999 [54] Niger, Sahel 13 11 2 – – n.s. 5 sites à 5 samples

Büdel et al., 2008 [17] South Africa 119 58 30 26 5 225 cm2 28 sites à 15 samples

Eldridge and Koen, 1998 [24] Eastern Australia 46 – – 24 22 500 cm2 282 sites

Eldridge et al., 2006 [22] Eastern Australia 50 – – 24 26 500 cm2 35 sites

C cyanobacteria, A eukaryotic algae, L lichens, B bryophytes, CZ Czech Republic, NV Nevada, UT Utah, AZ Arizona, NM New Mexico, NDNorth Dakota, FL Florida, n.s. not specifieda cyanobacteria + algae

404 T. M. Langhans et al.

Both stages of BSCs (initial and stable) are diversity“hot spots” with about 29 species of all studied taxa per20×20 cm plot.

Hypothesis 4

The nutrient contents of BSCs were low and habitat-typical(compare [9]). The extractable phosphate-P contents of initialand stable BSCs were similar and below the critical value of20 mg kg−1; therefore, ruderalisation will not occur [64].Total N, nitrate N, and total mineral N were low as well andnot significantly different between the crust types. Normally,the nutrient contents will increase with the progress ofsuccession (e.g., [65]). According to our results, we cannotconfirm this hypothesis; the age difference between our twostages is probably not sufficient to show such an increase.

An increase in the chlorophyll content as proposed byBüdel et al. [17] was also not found for our system. Thecontent of chlorophyll a in the micro-crusts showed nosignificant differences between initial and stable BSCs. In ourstudy area, the BSCs are different in their species composi-tion, but the chlorophyll a content is dependent on organisms'densities. The protonema was still in the substrate, andtherefore, it contributed chlorophyll a to the extract.

The measured contents are relatively low when com-pared to other studies. Lange [44] described maximalchlorophyll contents up to 100 mg m−2 for cyanobacteria/eukaryotic algae crusts, whereas BSCs including lichen orbryophyte material reached chlorophyll a contents above900 mg m−2. Furthermore, variations also occur betweencrusts of the same type. Lange et al. [46] reported achlorophyll density in lichen soil crusts from the NamibDesert varying between 200 and 500 mg m−2. Lowercontents, about 15–60 mg m−2, were shown by Kidron [41]in samples out of the Negev Desert.

Some authors reported that there were no differences inchlorophyll content between crusts of different crustedareas (e.g., [66]).

Acknowledgments The study was carried out with the support ofa PhD grant by the Darmstadt University of Technology. We thankProf. Dr. B. Büdel (Kaiserslautern) for most valuable helpconcerning the study and determination of BSCs and UrsulaLebong for technical assistance. The improvement of the Englishtext by Dr. A. Thorson (Oxford) is much appreciated. Especially,thanks to the “Regierungspräsidium Darmstadt” for permission towork in the area.

References

1. Ambos R, Kandler O (1987) Einführung in die Naturlandschaft.Mainzer Naturwissenschaftliches Archiv 25:1–28

2. Arnon DI (1949) Copper enzymes in isolated chloroplasts.Polyphenoloxidase in Beta vulgaris. Plant Physiol 24(1):1–14

3. Bailey D, Mazurak PA, Rosowski JR (1973) Aggregation of soilparticles by algae. J Phycol 9:99–101

4. Bazzaz FA (1975) Plant species diversity in old-field successionalecosystems in southern Illinois. Ecology 56:485–488

5. Belnap J, Eldridge DJ (2001) Disturbance and recovery ofbiological soil crusts. In: Belnap J, Lange OL (eds) Biologicalsoil crusts: structure, function, and management. Springer, Berlin

6. Belnap J, Gardner JS (1993) Soil microstructure in soils of theColorado Plateau: the role of the cyanobacterium Microcoleusvaginatus. Gt Basin Nat 53:40–47

7. Belnap J, Harper KT, Warren SD (1993) Surface disturbance ofcryptobiotic soil crusts: nitrogenase activity, chlorophyll content,and chlorophyll degradation. Arid Soil Res Rehab 8:1–8

8. Belnap J, Lange OL (2001) Biological soil crusts: structure, function,and management. Ecological studies 150. Springer, Berlin, p 503

9. Bergmann, S (2004) Zum Nährstoffhaushalt in Sandökosystemender nördlichen Oberrheinebene: Sukzession, Ruderalisierungspro-zesse und Effekte von Schafbeweidung. PhD Thesis, DarmstadtUniversity of Technology, Germany

10. Bhatnagar A, Makandar MB, Garg MK, Bhatnagar M (2008)Community structure and diversity of cyanobacteria and greenalgae in the soils of Thar Desert (India). J Arid Environ 72:73–83

11. Bischoff HW, Bold HC (1963) Phycological studies. IV. Some soilalgae from enchanted rock and related algal species. Univ TexasPubl 6318:1–95

12. Bliss LC, Gold WG (1999) Vascular plant reproduction,establishment, and growth and the effects of cryptogamic crustswithin a polar desert ecosystem, Devon Island, N.W.T., Canada.Can J Bot 77:623–636

13. Booth WE (1941) Algae as pioneers in plant succession and theirimportance in erosion control. Am J Bot 22:38–46

14. Breen K, Lévesque E (2006) Proglacial succession of biologicalsoil crusts and vascular plants: biotic interactions in the HighArctic. Can J Bot 84:1714–1731

15. Brooker RW, Maestre FT, Callaway RM, Lortie CL, CavieresLA, Kunstler G, Liancourt P, Tilebörger K, Travis JMJ,Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E,Kikvidze Z, Olofsson J, Pungnaire F, Quiroz CL, Saccone P,Schiffers K, Seifan M, Touzard B, Michalet R (2008) Facilita-tion in plant communities: the past, the present, and the future. JEcol 96:18–34

16. Büdel B (2001) Synopsis: comparative biogeography of soil-crustbiota. In: Belnap J, Lange OL (eds) Biological soil crusts: structure,function, and management. Springer, Berlin, pp 141–152

17. Büdel B, Darienko T, Deutschewith K, Dojani S, Friedl T, Mohr KI,Salisch M, Reisser W, Weber B (2009) Southern African biologicalsoil crusts are ubiquitous and highly diverse in drylands, beingrestricted by rainfall frequency. Microb Ecol 57(2):229–247

18. Cabała J, Rahmonov O (2004) Cyanophyta and algae as animportant component of biological crust from the PustyniaBłędowska Desert (Poland). Polish Bot J 49(1):93–100

19. Connell JH, Slatyer RO (1977) Mechanisms of succession innatural communities and their roles in community stability andorganization. Am Nat 111:1119–1144

20. Delgadillo C, Zander R (1984) The mosses of the Tehuacán Valley,Mexico, and notes on their distribution. Bryologist 87:319–322

21. Eckert RE, Peterson FF, Meurisse MS, Stephens JL (1986)Effects of soil-surface morphology on emergence and survival ofseedlings in big sagebrush communities. J Range Manag39:414–420

22. Eldridge DJ, Freudenberger D, Koen TB (2006) Diversity andabundance of biological soil crust taxa in relation to fine andcoarse-scale disturbances in a grassy eucalypt woodland in easternAustralia. Plant Soil 281:255–268

Community Assembly of Biological Soil Crusts 405

23. Eldridge DJ, Greene RS (1994) Microbiotic soil crusts: a reviewof their roles in soil and ecological processes in the rangelands ofAustralia. Aust J Soil Res 32:389–415

24. Eldridge DJ, Koen TB (1998) Cover and floristics of microphyticsoil crusts in relation to indices of landscape health. Plant Ecol137:101–114

25. Ettl H, Gärtner G (1995) Syllabus der Boden-, Luft- undFlechtenalgen. Fischer, Stuttgart, Jena, New York 721 pp

26. Flechtner VR, Johansen JR, Clark WH (1998) Algal compositionof microbiotic crusts from the central desert of Baja California,Mexico. Gt Bas Nt 58(4):295–311

27. Frahm J-P, FreyW (2004) Moosflora, 4th edn. Ulmer, Stuttgart, p 53828. Foster BL, Tilman D (2000) Dynamic and static views of

succession: testing the descriptive power of the chronosequenceapproach. Plant Ecol 146:1–10

29. Garcia-Pichel F, López-Cortés A, Nübel U (2001) Phylogeneticand morphological diversity of cyanobacteria in soil desertcrusts from the Colorado Plateau. Appl Environ Microbiol 67(4):1902–1910

30. Geitler L (1932) Cyanophyceae. Dr. L. Rabenhorst'sKryptogamen-Flora von Deutschland. Österreich und derSchweiz. 14. Band: Die Algen. Akademische Verlagsgesellschaft,Leipzig, p 1196

31. Hach T, Büdel B, Schwabe A (2005) Biologische Krusten inbasenreichen Sand-Ökosystemen des Koelerion glaucae-Vegetationskomplexes: taxonomische Struktur und Empfin-dlichkeit gegenüber mechanischen Störungen. Tuexenia25:357–372

32. Hahn A, Kusserow H (1998) Spatial and temporal distribution ofalgae in soil crusts in the Sahel of W Africa: preliminary results.Willdenowia 28:227–238

33. Harper KT, Marble JR (1998) A role for nonvascular plants inmanagement of arid and semiarid rangelands. In: Tueller BT(ed) Vegetation science applications for rangeland analysis andmanagement. Kluwer Academic Publishers, Dortdrecht, Bos-ton, London, p 656

34. Harper KT, Pendleton RL (1993) Cyanobacteria and cyanolichenscan they enhance availability of essential minerals for higherplants? Gt Basin Nat 53:59–72

35. Hawkes CV, Flechtner VR (2002) Biological soil crusts in axeric Florida Shrubland: composition, abundance, and spatialheterogeneity of crusts with different disturbance histories.Microbial Ecol 43:1–12

36. Jafari M, Tavili A, Zargham N, GhA H, Zare Chahouki MA,Shirzadian S, Azarnivand H, GhR Z, Sohrabi M (2004)Comparing some properties of crusted and uncrusted soils inAlagol Region of Iran. Pakistan J Nutrition 3:273–277

37. Johansen JR (1993) Cryptogamic crusts of semiarid and arid landsof North America. J Phycol 29:140–147

38. Johansen JR, Ashley J, Rayburn WR (1993) Effects of rangefireon soil algal crusts in semiarid shrub-steppe of the lowerColumbia basin and their subsequent recovery. Gt Basin Nat53:73–88

39. Johansen JR, St Clair LL, Webb BL, Nebekter GT (1984)Recovery patterns of cryptogamic soil crusts in desert rangelandsfollowing fire disturbance. Bryologist 87:238–243

40. Kaštovská K, Elster J, Stibal M, Šantrůčková H (2005)Microbial assemblages in soil microbial succession afterglacial retreat in Svalbard (High Arctic). Microb Ecol50:396–407

41. Kidron GJ (2007) Millimeter-scale microrelief affecting runoffyield over microbiotic crust in the Negev Desert. Catena70:266–273

42. Komárek J, Anagnostidis K (1999) Süßwasserflora von Mitteleur-opa 19/1. Cyanoprokaryota, 1. Teil: Chroococcales. Spektrum,Heidelberg, p 548

43. Komárek J, Anagnostidis K (2005) Süßwasserflora von Mitteleur-opa 19/2. Cyanoprokaryota, 2. Teil: Oscillatriales. Spektrum,Heidelberg, p 759

44. Lange OL (2001) Photosynthesis of soil-crust biota as dependenton environmental factors. In: Belnap J, Lange OL (eds) Biologicalsoil crusts: structure, function, and management. Springer, Berlin,pp 217–240

45. Lange OL, Kidron GJ, Büdel B, Meyer A, Kilian E, Abeliovich A(1992) Taxonomic composition and photosynthetic characteristicsof the “biological soil crusts” covering sand dunes in the westernNegev Desert. Func Ecol 6:519–527

46. Lange OL, Meyer A, Zellner H, Heber U (1994) Photosyn-thesis and water relations of lichen soil crusts: field measure-ments in the coastal fog zone of the Namib Desert. Func Ecol8:253–264

47. Langhans TM, Storm C, Schwabe A (2009) Biological soil crustsand their microenvironment: impact on emergence, survival andestablishment of seedlings. Flora 204(2):157–168

48. Langhans TM, Storm C, Schwabe A (2010) Regenerationprocesses of biological soil crusts, macro-cryptogams andvascular plant species after fine-scale disturbance in a temper-ate region: recolonization or successional replacement? Flora205(1)

49. Lesica P, Shelly JS (1992) Effects of cryptogamic soil crust on thepopulation dynamics of Arabis fecunda (Brassicaceae). Am MidlNat 128:53–60

50. Loucks OL (1970) Evolution of diversity, efficiency, andcommunity stability. Am Zool 10:17–25

51. Lukešová A (2001) Soil algae in brown coal and lignite post-mining areas in Central Europe (Czech Republic and Germany).Restor Ecol 9(4):341–350

52. Lukešová A, Hoffmann L (1996) Soil algae from acid rainimpacted forest areas of the Krušné hory Mts. 1. Algalcommunities. Vegetatio 125:123–136

53. Lukešová A, Komárek J (1987) Sucession of soil algae on dumpsfrom strip coal-mining in the Most Region (Czechoslovakia).Folia Geobot Phytotaxon 22:355–362

54. Malam Issa O, Trichet J, Défarge C, Couté A, Valentin C(1999) Morphology and microstrucutre of microbiotic soilcrusts on a tiger bush sequence (Niger, Sahel). Catena 37:175–196

55. Mazor G, Kidron GJ, Vonshak A, Abeliovich A (1996) The roleof cyanobacterial exopolysaccharides in structuring desert micro-bial crusts. FEMS Microb Ecol 21:121–130

56. Pluis JLA (1994) Algal crust formation in the inland dune area,laarder Wasmeer, the Netherlands. Vegetatio 113:41–51

57. Rayburn WR, Mack RN, Metting B (1982) Conspicuous algalcolonization of the ash from Mount St. Helens. J Phycol18:537–543

58. Rippka R, Desrulles J, Waterbury JB, Herdman M, Stanier RY(1979) Genetic assignment, strain histories and properties of purecultures of cyanobacteria. J Gen Microb 11:1–61

59. Rivera-Aguilar V, Montejano G, Rodríguez-Zaragoza S,Durán-Díaz A (2006) Distribution and compaosition ofcyanobacteria, mosses and lichens of the biological soil crustsof the Tehuacán Valley, Puebla, México. J Arid Environ67:208–225

60. Ronen R, Galun M (1984) Pigment extraction from lichens withdimethyl sulfoxide (DMSO) and estimation of chlorophylldegradation. Environ Exp Bot 24:239–245

61. Schoonmaker P, McKee A (1988) Species composition anddiversity during secondary succession of coniferous forests inthe western Cascade Mountains of Oregon. For Sci 34:960–979

62. Shields LM, Drouet F (1962) Distribution of terrestrial algaewithin the Nevada Test Site. Am J Bot 49:547–554

406 T. M. Langhans et al.

63. Shubert E, Starks TL (1980) Soil–algal relationships from surfacemined soils. Br Phycol J 15:417–428

64. Süss K, Storm C, Zehm A, Schwabe A (2004) Succession in inlandsand ecosystems: which factors determine the occurrence of the tallgrass speciesCalamagrostis epigejos (L.) Roth and Stipa capillataL.? Plant Biol 6:465–476

65. Tilman D (1987) Secondary succession and the pattern of plantdominance along experimental nitrogen gradients. Ecolog Monogr57:189–214

66. Tirkey J, Adhikary SP (2005) Cyanobacteria in biological soilcrusts of India. Curr Sci 89(3):515–521

67. VDLUFA (Verband der landwirtschaftlichen Untersuchungs-und Forschunganstalten) (1991) Methodenbuch. Band 1. DieUntersuchung von Böden, 4th edn. VDLUFA-Verlag,Darmstadt

68. Whittaker RH (1972) Evolution andmeasurement of species diversity.Taxon 21:213–251

69. Wirth V (1995) Flechtenflora, 2nd edn. Ulmer, Stuttgart, p 661

Community Assembly of Biological Soil Crusts 407