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Importance of biological loess crusts for loess formation in semi-aridenvironments

Zorica Svir�cev a, Slobodan B. Markovi�c a,*, Thomas Stevens a,b, Geoffrey A. Codd c, Ian Smalley d,Jelica Simeunovi�c a, Igor Obreht a, Tamara Duli�c a, Dijana Panteli�c a, Ulrich Hambach e

a Laboratory for Paleoenvironmental Reconstruction, Faculty of Sciences, University of Novi Sad, Trg D. Obradovi�ca 2, 21000 Novi Sad, SerbiabCentre for Quaternary Research, Department of Geography, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UKcBiological and Environmental Sciences, School of Natural Sciences, University of Stirling, Stirling FK9 4LA, UKdGiotto Loess Research Group, Department of Geology, Leicester University, LE1 7RH, UKeChair of Geomorphology, University of Bayreuth, 95440 Bayreuth, Germany

a r t i c l e i n f o

Article history:Available online 30 October 2012

a b s t r a c t

The essential abiotic components for loess formation are: material (dust), atmospheric circulation(wind), suitable surface conditions for the trapping of aeolian material, and for the subsequent devel-opment of typical loess sedimentary structures. In spite of the world-wide distribution of loess deposits,knowledge of the processes of dust accumulation and its transformation to mature loess sediment is stillinadequate. Loess accumulation appears greatest during the most arid periods and in semi-arid regions.Biological crusted surfaces (BCS) are of potentially great importance in loess formation, especially insemi-arid regions. BCS are highly specialized extremophile communities and apparently play animportant role in atmospheric dust trapping and erosion prevention. Results indicate that cyanobacterialstrains isolated from current Carpathian Basin loess exhibit specific morphological and eco-physiologicalcharacteristics that play a key role in loess formation, warranting adoption of the new term biologicalloess crusts (BLC). A model of the influence of cyanobacterial BLC life strategies on loess formationexplains trapping, accumulation and preservation, as well as loess texture and structure. This potentialsignificance of BLC in the accumulation and preservation of loess sediments may be considered asa model suitable model database for recognition of bioorganic modification of geological strata. Myco-sporine and scytonemin pigments can serve as BLC biomarkers, elucidating their role in soil evolutionand in aiding paleoclimatic, paleoenvironmental and paleovegetation reconstructions.

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1. Introduction

Loess is one of the most widespread continental sedimentaryformations of the Quaternary, covering about 10% of the currentland surface. The majority of these wind-blown deposits areconcentrated in semi-arid regions of inner Eurasia (Smalley et al.,2011). Loess sedimentation is dominantly Quaternary in age, butin China loess or loess-like sequences potentially extend to the baseof the Miocene (Guo et al., 2002). By contrast, lithified loess (loes-site) is relatively rare in the pre-Quaternary geologic record,although this may to some extent be an artefact of difficulty in

identification (Johnson, 1989). Loessite has been reported from thelate Paleozoic of equatorial Pangaea, currently located in NorthAmerica (Soreghan et al., 2002), and even in the Precambrian ofnorth Norway (Edwards, 1979). In spite of the world-wide distri-bution of loess deposits, and a vast literature dedicated to theirpalaeoclimatic interpretation, knowledge of the processes oftransformation from accumulated dust, via stabilisation, to matureloess sediment is still relatively poor. In essence, we lack a widelyapplicable model for loess formation. For example, wind is crucialfor the deposition of aeolian material, but simultaneously in thecase of weak vegetation cover, wind can be a major erosive force(Stevens et al., 2006, 2008). This apparent paradox can be resolvedby evoking specific conditions at the sediment surface that areconducive to dust trapping and sedimentation. While this hastraditionally focussed on vegetation (Tsoar and Pye, 1987; Daninand Ganor, 1991), it remains unclear how this would occur insemi-arid regions during cold and dry glacial periods associated

Abbreviations: BCS, biological crusted surfaces; BSC, biological soil crusts; BLC,biological loess crusts; BLOCDUST model, Biological LOess Crusts Dust Trappingmodel.* Corresponding author.

E-mail address: slobodan.markovic@dgt.uns.ac.rs (S.B. Markovi�c).

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with weak vegetation cover. These environmental conditions arethought to have been dominant at times and places of high loessformation rates. Here, it is proposed that stabilization of depositedaeolian dust into loess could be achieved by the participation ofhighly specialised extremophile microbiological loess surfacecommunities. Their closest recent environmental equivalents arebiological soil crusts (BSC) which frequently occur in current warmand cold, arid and semi-arid regions (e.g. Belnap and Lange, 2001;Chen et al., 2012).

The aim of this study is to introduce a new concept of loessformation by biological loess crusts (BLC), as previously noted bySmalley et al. (2011), and evaluate its potential importance in semi-arid regions. Finally, a novel conceptual model of dust trappingcontrolled by eco-physiological activity of BLC microorganisms isintroduced, with data from preliminary biomarker experiments totest their past presence.

2. Loess formation e what is missing?

Loess can be loosely defined as homogeneous, typically non-stratified, porous, friable, slightly coherent, often calcareous, fine-grained, silty, pale yellow or buff, wind-blown (aeolian) sediment.It consists of mainly quartz particles concentrated in the size range10e75 mm, where silt makes up 40e70% by weight (Pécsi, 1990,1995; Smalley, 1995; Smalley et al., 2011). In addition to thepredominant quartz grains (40e80%; on average, 60e70%), loesscontains feldspars, micas, calcite and dolomite in lesser amounts,with varying amounts of heavy minerals. The coarse granulartexture of loess due to the cohesion and cementation of grains(described below) is also very characteristic (Pecsi, 1995). Itgenerally occurs as a widespread blanket deposit that covers areasof hundreds to thousands of square kilometres and reaches thick-nesses of tens to hundreds of metres (Pécsi, 1990; Smalley et al.,2011). As noted above, while widespread in the Quaternary, pre-Quaternary loess is far more restricted, potentially in part due todifficulties in identification.

The formation of a loess deposit is a complex process, or caneven be considered as the culmination of a complex series ofprocesses. The basic requirements for loess deposition are: 1)a source of material (dust), 2) an atmospheric transport mechanism(wind) and 3) appropriate boundary layer and Earth-surfaceconditions for trapping and transforming aeolian material intodeposited loess sediment (deposition and diagenesis). The forma-tion of the particles is not a straightforward event and discussion onthis topic is currently occurring in many loess regions (e.g. Újváriet al., 2008, 2012; Stevens et al., 2010) and will not be discussedhere. The aeolian transport event remains central to the formationof a loess deposit, and this realisation was the most importantmoment in the history of loess research (Smalley et al., 2011).Equally as significant in allowing loess formation is the process ofdeposition. There are three ways to deposit subaerial material: 1)a reduction in the power of transporting agent (i.e., a dropping ofwind speed, i.e., dry deposition); 2) incorporation of dust particleinto water droplet and precipitation (wet deposition) and; 3)trapping of particles due to local boundary layer conditions.Traditionally, specific types of vegetation have been regarded as keyto trapping of dust and a pre-requisite for arid to semi-arid loessdeposition, where wet deposition is negligible and wind speedsremain high (Tsoar and Pye, 1987).

However, Pécsi (1990) argued that there is more to loessformation than simply aeolian dust trapping and deposition. He re-introduced the term loessification (the concept was originallyBerg’s idea; see Smalley et al., 2010, 2011) to describe the integratedset of all post-depositional processes related to the transformationof wind-blown silty material to a well-sorted open structured

deposit with classic loessic properties (Smalley and Markovi�c, inpreparation). The idea of loessification has become more attrac-tive now that some attention is being focused on processes whichoccur after aeolian deposition, and before actual observation of thedeposit. Three aspects of post-aeolian loessification can be identi-fied: formation of fine calcite and other carbonates at particleinterstices in the deposit; formation of clay minerals in the sameinterparticle zones (Smalley and Markovi�c, in preparation) andpioneer biological colonisation, perhaps largely driven by cyano-bacterial activity (Smalley et al., 2011).

In previous interpretations, the third, biotic aspect of loessifi-cation has not been described, and the event was described mostlyas a complex of predominantly abiotic processes (Berg, 1916;Ambro�z, 1947; Lo�zek, 1965; Smalley, 1975; Pécsi, 1990; Cilek, 2001).By contrast, depositional processes involve interaction betweenabiotic and biotic elements. In classical studies, this has often beenlimited to the importance of local vegetation development in loessformation (e.g. Lo�zek, 1965). However, since wind can also bea major erosive force in dynamic terrestrial environments, such asglacier-marginal zones and arid to semi-arid continental regions,weak or limited vegetation cover does not seem likely to provideadequate protection for deflation. Furthermore, these zones areprecisely where vegetation would be limited, allowing wind- andwater-driven erosion to dominate. For example, during glacialclimatic conditions vegetation can become quite reduced inresponse to extreme environments, forming ecosystems such asloess tundra (Lo�zek, 1964; Moine et al., 2008) or dry, poorlydeveloped loess grassland (Markovi�c et al., 2006, 2007, 2008).However, at precisely the time vegetation was most limited, thethickest European lower last glacial loess deposits are preserved innorthern Serbia (Vojvodina). In Vojvodina, this loess layer (V-L1L2;approximately equivalent to Marine Isotope Stage 4) can exceed4 m thickness (Antoine et al., 2009; Bokhorst et al., 2011). Lumi-nescence dating suggests some of the highest rates of loess sedi-mentation over the last glacial interglacial cycle for this period(Stevens et al., 2011). Malacological investigations of loess unit V-L1L2 indicate that the period of its formation was the driest part ofthe last glacial phase. Identification of a very small total number ofpreserved fossil snail shells (in some samples no shells wereobserved), mostly xerophytes, indicate the presence of very weakgrassy vegetation cover (Markovi�c et al., 2005, 2006, 2007, 2008).These results are in agreement with independent investigations oflong-chain, plant-derived n-alkane biomarkers (Zech et al., 2009).

This discussion raises two clear questions: 1) does weak xero-phylic grass cover provide suitable conditions for trapping andpreserving of airborne dust, to the extent that near continuous andhigh sedimentation rate loess deposits are formed? 2) Do tradi-tional models of loessification fully explain the particular structureof loess rather than simple wind-blown dust?

3. Biological crusted surfaces (BCS)

The apparent paradox implicit in the first question can beresolved by evoking recent studies by Xu and Chen (2008) andSmalley et al. (2011), which suggest that the eco-physiologicalactivities of microorganisms such as cyanobacteria, lichens,mosses and fungi can potentially play an important role in trans-formation of aeolian dust into loess sediments. These organismscan form biological crusted surfaces (BCS) (Fig. 1): highly special-ized, resilient communities which currently occur inwarm and coldarid and semi-arid regions, and other extreme habitats such assteep loess cliffs and desert environments (Starks et al.,1981; Büdel,2002; Metcalf et al., 2012). BCS are very specialized biotopes withdifferent communities of species mainly determined by substratequality and quantity.

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Most often these biocenoses appear as biological soil crusts(BSC), which are very well known and described (Wynn-Williamset al., 2000; Belnap and Lange, 2001; Belnap et al., 2006). BSC areformed by the actions and by-products of living organisms, whichcreate a crust of soil particles bound together by organic materials(Belnap et al., 2001). BSC are highly specialized communities ofspecies of cyanobacteria, green algae, lichens, mosses, microfungiand bacteria (Belnap, 2001; Belnap et al., 2001; Ullmann and Büdel,2001; Tirkey and Adhikary, 2005; Bowker et al., 2008). They arewidely found at different surfaces in nature, very often as pioneerorganisms (Whitton and Potts, 2003). The biomass of organismspresent in BSC reflects the climate at the site, the time since pastdisturbance, and the severity of that disturbance. In hot desertswith very low precipitation, biological soil crusts are dominated bya low amount of cyanobacteria (Belnap et al., 2006).

Belnap and Lange (2001) summarized the results of manystudies on biological soil crusts and reported that airborne silt andclay particles suspended in a dusty atmosphere can be trapped bysticky cyanobacterial sheaths, by frost-heaved surfaces and byprotruding moss stems and lichen thalli. Material blowing acrossbiological soil crusts can become trapped, either accumulatingwithin low pockets in themicrotopography, or mostly by sticking tothe exudates of cyanobacterial sheaths. These organisms includephototropic filamentous forms which, if not buried too deeply, willpush by gliding motion through loose soil and organic matter,further trapping or entangling soil in the process (Fryberger et al.,1988; Campbell et al., 1989; Gillette and Dobrowolski, 1993). Bothfilamentous and unicellular crust-forming cyanobacteria producesheaths or capsules of extracellular polysaccharides (EPS). Thesecarbohydrates aid in soil aggregation by cementing particlestogether (Van den Ancker et al., 1985; Danin et al., 1989; Chartes,1992; Belnap and Gardner, 1993; Eldridge and Greene, 1994;Wynn-Williams et al., 2000; Belnap, 2003; Belnap et al., 2003). Thecollection of airborne silt particles is a part of the life strategy of soilcrust organisms. In taking particles as a source of mineral materialfor their metabolism, soil crust organisms significantly increase soilfertility and water-holding capacity. The cyanobacterial communi-ties can potentially add further to soil fertility since some species

can fix atmospheric nitrogen. Many studies have shown that thepresence of biological soil crusts reduces soil erosion by wind(Dulieu et al., 1977; Gillette et al., 1980; Van den Ancker et al., 1985;Tsoar and Møller, 1986; Danin et al., 1989; Pluis, 1994; Williamset al., 1995; Belnap and Gillette, 1997; Marticorena et al., 1997;Belnap and Gillette, 1998; Leys and Eldridge,1998; Musick,1998). Inaddition, further ecological functions of BSC also include:increasing soil stability, improving soil fertility (nutrient contribu-tions to plants), preventing water erosion, atmospheric nitrogen-fixation, soil-plant-water relations, etc. (Belnap et al., 2006).

4. Biological loess crusts and loess formation

A biological loess crust (BLC) is one specific type of BCS, and ithas been suggested that they might present very significantbiomass at the loess surfaces (Smalley et al., 2011). Preliminaryresults from Serbian loess samples show that BLC are comprised ofabout 90% of cyanobacterial biomass (Nostoc, Phormidium, Gloeo-capsa, Stigonema, Oscillatoria) and 10% of other BLC organisms,mostly bacteria (Fig. 1).

In some cyanobacteria, rehydration rather than desiccationappears to be a fatal event. To protect the cells during rehy-dratation, a water stress protein and large amounts of the sugartrehalose are synthesized that stabilize the phospholipid bilayers ofcellular membranes (Potts, 1996, 1999; Qiu et al., 2004). Stickypolysaccharide sheaths exuded around cyanobacterial cells aid inloess aggregation by catching and cementing particles together(Fig. 1). Biofilm exuded by cyanobacteria and green algae, incombination with lichens and moss rhizomes, entrap and bindsediment particles together, increasing the size of particle aggre-gates (Smalley et al., 2011). As particle aggregates are enlarged, theybecome heavier, have a relatively smaller surface area, and aremore difficult for wind or water to move (Danin and Yaalon, 1980;Danin et al., 1989).

At the same time, captured silt particles increase water-holdingcapacity and provide necessary mineral nutrients for furthergrowth of the BLC. The clay particles are negatively charged andbind positive cationic nutrients (e.g. K, Ca2) preventing them from

Fig. 1. BCS in the Vojvodina region (North Serbia).

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leaching into the subsoil. Simultaneously, the BLC prevents defla-tion of the deposited dust by forming a protective crusted surface.Subsequently, lichens, fungi and moss establish themselves in thecrust, enriching and stabilizing the soil. Increased bioavailability ofnitrogen during drought is related to disintegration and lysis ofcyanobacterial material. In the absence of native or naturalised N2-fixing plants, cyanobacterial crusts are likely to be significantcontributors to nitrogen pools, particularly during drought(Williams and Eldridge, 2011).

Together with captured silt particles, the presence of cyano-bacterial EPS in crusted surfaces decreases soil or loess perme-ability. For example, cyanobacterial components of biological soilcrusts rapidly swell up to 13 times their dry volume (Shields andDurrell, 1964; Campbell, 1977), potentially closing flow pathwaysthrough the soil surface. This process could also contribute toformation of loess structure.

The process of loess deposition and preservation might beheavily influenced by themetabolic activity of BLCmicroorganisms,mainly through BLC polysaccharides (Fig. 2). The sticky poly-saccharide material on the topographic surface, exuded mostly bycyanobacteria, can trap silty particles suspended in a dusty atmo-sphere (Fig. 3B,D,F-BLC glue) (Fig. 3). This collection of airborneloess-forming particles (ALFP) is part of the life strategy of crustorganisms in so far as they provide the necessary minerals forfurther growth of the BLC, which in turn provides protection fromdesiccation during dry periods. Simultaneously, polysaccharidessecreted by crust organisms bind particles inside the BLC zone,forming a cohesive crust that resists both wind and water erosionduring dry periods (Fig. 3A,C,E-BLC net). Metabolized particles(Fig. 3:MLFP), together with exuded metabolites (Fig. 3:BLCM) andunused airborne particles (Fig. 3:ALFP) become the uppermostloess sediment covered with BLC (Fig. 3C,E). Every year duringmoist seasons (Fig. 3), the accumulation of dust and loess-formingparticles is very active (Fig. 3B,D,F). During dry phases (Fig. 3), theBLC becomes very stable and develops a resistant surface pre-venting wind and water erosion (Fig. 3A,C,E). The drying periodinduces polysaccharide production by cyanobacteria, serving to asprotecting molecules from water stress. In the presence of waterduring a moist phase, polysaccharides produced in the transitionfrom wet to dry phases and accumulated during dry phases to

become a new sticky layer for dust accumulation and initiate a newcycle of loessification (Fig. 3B,D,F).

This model suggests that loess formation is intimately tied toBLC and cyanobacterial activity, preferably combined with dry andwet environmental shifts. This scenario might describe not onlytrapping, deposition and preservation, but also might shed lighton loess granulometry, thickness, permeability, geographicalzonation, adaption to the landscape and its changeabilityunder human influence. Since BLC can be highly influenced bylocal changes of mineral and organic compounds, as well asmoisture and temperature, this observation also raises questionsabout the importance of local environmental conditions for loessdeposition.

Given that BLC is common on current loess surfaces that formthe first stages of vegetation succession and also plays a key role inpreventing wind and water erosion on disturbed soil, the proposedscenario about BLC-dependent loessification should thus be seri-ously considered as one of the fundamental requirements for loessformation in semi-arid areas.

Fig. 4 presents different types of dry and wet phases of cyano-bacteria isolated BLC surfaces from several localities in the Vojvo-dina region. Transformation from dry to wet phase is relativelyquick process under laboratory as well as in natural conditions.

5. BLC biomarkers and paleoenvironmental reconstruction

Generally, loess has some “life friendly” characteristics similar tosoils, including fertility (physiologically available mineral nutrientsdue to its aeolian origin) and porosity. With respect to these char-acteristics, loess substrate can be rapidly transformed to soil undercertain climatic and environmental conditions. Offering variousliving niches, even in unfavourable environmental conditions, loesscan be described as a pedoregolith. Living in the BLC, cyanobacteriaand other microorganisms contribute a range of characteristic,extracellular metabolic products to the matrix (Fig. 3: BLCM). Someof these products are resistant to degradation and can serve asmarkers of the previous presence of the microbes, and by exten-sion, BLC. If those metabolites are species- or group-specific, theymight be used as good biomarkers regarding paleoclimatic andpaleoenvironmental conditions.

Fig. 2. Extracellular polysaccharide sheath material (EPS) exuded by BLC cyanobacteria (C). (Photo Miroslav Gantar).

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A biomarker is a compound that could indicate the biologicalorigin of organic matter. Once the molecular structure and isotopiccomposition are identified, the source of the biomarkers and theircompositional character and distribution pattern can be deter-mined to genus or species level. Molecular fossils have been appliedin the studies on paleoenvironmental and paleoclimatic changes inloess-paleosol sequences (Xie et al., 2002; Wang et al., 2004; Zhanget al., 2008; Zech et al., 2009). Edwards et al. (2005) reported theresults of experiments on extant Antarctic extremophile cyano-bacteria using a range of Raman excitation wavelengths in detec-tion of molecular spectral biosignatures, which may be consideredas a suitable database for the recognition of bioorganic modifica-tion of geological strata. There has been considerable interest byorganic geochemists in lipids of cyanobacteria since these organ-isms are known to have been significant sources of organic matterin many sediments throughout geological time, for example invarious types of living- to fossil lake sediments and cyanobacterialmats (Awramik, 1984; Dobson et al., 1988; Robinson and Eglington,1990; Shiea et al., 1990; Kenig et al., 1995). Different extant forms ofancient cyanobacteria have been shown to contain hydrocarbondistributions similar to those in sediments (Gelpi et al., 1970;Brassel, 1994; Summons, 1993). Cyanobacteria in BLC producea sticky biofilm mainly containing different polysaccharidesincluding a variety of short-chain (C7eC14) hydrocarbons as well asdifferent cyclopentanes and cyclohexanes (Gelpi et al., 1970;Grimalt et al., 1992; Dembitsky et al., 1999). Some short-chain(C16eC21) monomethylalkanes (MMAs) and dimethylalkanes(DMAs) are common in geological samples. These compounds havebeen identified in modern and Holocene microbial mats (Shieaet al., 1990; Kenig, 2000; Kenig et al., 1995), ancient sediments(Summons, 1987; Summons et al., 1988a,b; Summons and Walter,1990; Hold et al., 1999; Audino et al., 2001) and crude oils(Jackson et al., 1986; Fowler and Douglas, 1987; Kissin, 1987;Warton et al., 1997). They were also identified in growing cyano-bacterial cultures (Han et al., 1968; Gelpi et al., 1970; Koster et al.,1999; Dembitsky et al., 2001). Thus, when found in geologicalsamples, these compounds can serve as biomarkers for cyanobac-teria (e.g., Dachs et al., 1998). Branched alkanes and other apolarcompounds produced by the cyanobacteria have been recentlyinvolved in paleoclimatic reconstruction and extreme environmentinvestigation. n-alkanes are chemically and biologically resistantand are often found in sediments in quantities sufficient for analysisand because of that, they are also common biomarkers. Summonset al. (1999) discovered unique biomarkers for cyanobacterialoxygenic photosynthesis; 2-methylhopanes. Considering theiroccurrence in modern organisms, and their ancient sedimentarydistributions, 2-methyl- or 3-methylhopanes are proposed to bebiomarkers derived from cyanobacteria (Summons et al., 1999;Eigenbrode et al., 2008; Brocks et al., 1999, 2003).

In addition, cyanobacteria in crusts exposed to sunlight containextracellular UV-protective pigments, mycosporine, amino acid-likesubstances (MAAs) and different hopans, which can be determinedin fossil records (Cockell, 1998; Cockell and Knowland, 1999; Brockset al., 2003; Edwards et al., 2005). Thus, when found in geologicalsamples, these compounds can also serve as biomarkers for cyano-bacteria (e.g., Dachs et al., 1998). Mycosporine is a secondarymetabolite that appears exclusively in terrestrial isolates (Volkmannand Gorbushina, 2006; Palinska et al., 2011). Some other cyano-bacterial biomarkers are found in recent and ancient sediments:carotenoids and kerogens (Damste and Koopmans, 1997), porphy-rins (Huseby and Ocampo, 1997), hopanoids (Summons et al., 1999)and scytonemin, UV (370e384 nm) sunscreen pigment that accu-mulates in the cyanobacterial sheaths (Leavitt et al.,1997; Dillon andCastenholz, 1999; Balskus et al., 2011). Some specific cyanobacterialcarotenoids (echinenone) appear frequently in the form of rings and

Fig. 4. Isolated cyanobacteria from BLC e dry samples of BLC (a, c, e) with corre-sponding wet phases (b, d, f).

Fig. 3. Possible model of the influence of BLC on loess formation (Biological LOessCrusts Dust Trapping model e BLOCDUST model): A. Initial dry season e BLC netprevents accumulation (solid line) and deflation (dashed line); B. Initial wet season e

polysaccharide glue catches dust from air; C. and E. Next dry seasons e preservation ofaccumulated layers from previous wet seasons, i.e., no deflation; D and F. Next wetseasons e formation of new polysaccharide glue associated with collecting of dustfrom air and transformation of older layers of accumulated dust to proto-loessdeposits. BLC e biological loess crust; BLC glue e sticky polysaccharides producedby BLC organisms; ALFP e airborne loess-forming particles; MLFP emetabolized loess-forming particles; BLCM e metabolites, biomarkers.

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similar complex structures (as in isoprenoids)which retain their coreintegrity even when their side chains are degraded by microbialdecomposition or natural entropy (Palinska et al., 2011). The cores ofthesemolecules, suchas the tetrapyrrole ringof porphyrins, are goodbiomarkers for extant surface life in extremedesert habitats. Deamer(1997) puts the origin and fate of porphyrins into an astrobiologicalcontext. Wynn-Williams et al. (2002) suggested the UV protectantscytonemin, chlorophyll (essential primary photosyntheticpigment), C-phycocyanin (accessory light-harvesing pigment) anda hopanoid as typical biomarkers of astrobiological relevance inRamanspectral databases, since these pigmentswere extracted from2 � 0.5 Gyr microbial stromatolite material from Australia.

Preliminary analyses of cyanobacterial biomarkers in selectedsediment samples from Vojvodina have been performed at theLaboratory for Paleoenvironmental reconstruction, University ofNovi Sad (Serbia), using spectrophotometric methods and flowcytometry (unpublished data). Preliminary pigment analysis resultsfrom 6 loess samples taken at Roguli�c gully profile near Mo�sorinvillage at Titel loess plateau (Bokhorst et al., 2011; Gaudenyi et al.,2011). Samples cover a time slice from the Early to the latest Plen-iglacial period and show the presence of cyanobacterial UV-photoprotective pigments: mycosporines and scytonemins. Thesepigments have a structure with components which are frequentlyrings (as in isoprenoids) which retain their core integrity. Themolecular structures of these pigments are relatively stable andtheir degradation in cells is a very slow process. The cores of thesepigments are good biomarkers for extant surface life in extremedesert habitats (McKay, 1997). Pigments such as scytonemins andmycosporines therefore have greater potential as biomarkers inpaleoclimate reconstruction, as compared to photosyntheticpigments such as C-phycocyanin and other phycobiliproteins (C-allophycocyanin and C-phycoerythrin) which were not found(Adhikary and Sahu, 1998) They are sensitive to the light environ-ment (irradiance and wavelength), and to nitrogen availability andmay thus change independently of biomass, and are best used asa relativemeasurewithin a single point in time (Bowkeret al., 2002).

Fig. 5 shows chronostratigraphy, grain size distribution, total landsnails abundance and mycosporine and scytonemin absorbancerecorded at the loess-paleosol sequence located in the Roguli�c gully

profile near Mo�sorin village at Titel loess plateau. The preliminaryresults suggest that concentrations of scytonemins andmycosporinesin loess samples vary significantly through time. The concentrationsof both UV-photoprotective pigments detected spectrophotometri-cally were in the same range. According to the relationship with totalabundance of identified land snail assemblages, a general proxy forhumid environments, scytonemin also can be regarded as a potentialindicator of dry conditions. However, these results were obtainedbefore necessary methodological improvements, and are still inade-quate for valid environmental interpretations.

6. Discussion

The BLOCDUST conceptual model of the role of BLC in loessformation provides a great opportunity to improve understandingof some important aspects of loess distribution, preservation,thickness, grain size composition, structure and paleoclimatic andpaleoenvironmental reconstruction.

6.1. Distribution, preservation and thickness

In spite of the high susceptibility of loess sediments to erosion,thick, mostly Pleistocene loess deposits are preserved over largeexpanses of the huge semi-arid zone of Eurasia. Quaternary loesscovers 10% of the world’s continents (Pye, 1984). In attainingconsiderable thicknesses of the order of 100 s of metres, andformed under high accumulation rates, they preserve long-termquasi continuous paleoclimate records that reveal millennial-scale climate changes (e.g. Ding et al., 2002; Stevens et al., 2007,2008; Dodonov and Zhou, 2008; Markovi�c et al., 2009, 2011).

Generally, the loess plateau deposition model applicable to themost significant Eurasian loess accumulations implies almostcontinuous aeolian dust accumulation. This has been linked tosemi-arid climate conditions and to limited post-depositionalerosion processes (e.g. Markovi�c et al., 2012). While fluvial(Markovi�c et al., 2008) and gully erosion (Porter and An, 2005),especially during interglacial phases, can contribute to a reductionin loess plateau spreading, there is a paradox inherent in theunderstanding of loess accumulation. Semi-arid regions may have

Fig. 5. Loess profile in the Roguli�c gully profile near Mo�sorin village at Titel loess plateau. Comparison between chronostratigraphy (Markovi�c et al., 2008), grain size distribution(Bokhorst et al., 2011), total land snails abundance (Gaudenyi et al., 2011) and preliminary results of mycosporine and scytonemin absorbance. Lithological interpretations accordingto Gaudenyi et al. (2011) are presented in legend and luminescence dates after Bokhorst et al. (2011).

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sparse vegetation and highly active aeolian activity. This implieslimited potential for accumulation, and particularly for preserva-tion, especially during cold and dry glacial phases. This is explainedthrough the presence of extensive BLC development in loessplateau environments during glacial phases. Abundant evidence forthe ability of cyanobacteria to grow at low temperature exists, forexample in Antarctic dry valleys (Vincent, 2000).

Strong climatic seasonality in the large inner Eurasian loess zonehas been reconstructedduring glacial phases (Machalett et al., 2008;Markovi�c et al., 2012). The most probable annual climatic scenariopoints to the existence of a relatively humid (melt) phase at the endof the long glacial winter, and very dry periods during the shortglacial summer. This scenario is extremely unfavourable for thedevelopment of glacial grassy vegetation on an accumulating loessplateau surface predisposed to weak vegetation cover. However,these extreme annual changes in glacial climate are associated withtwo different modes of the BLC eco-physiological annual cycle. Atthe beginning of the melt season, characterized by the existence ofinitial week vegetation, BLCs are dominant on the loess surface. Dueto much quicker eco-physiological response to the transition torelatively humid conditions of the BLC than of vascular plants(Belnap, 2001), sticky polysaccharides of BLC would be frequent atthe loess plateau surface, and be very efficient in collecting dustparticles from a windy dust-ridden atmosphere. This ‘active melt’phase is preciselywhen conditions for dust transportwould bemostfavourable as particles are liberated from frozen soils and sedimentaccumulations. During the drought peaks of glacial summer, vege-tation cover is weak and BLC cover a large part of the loess plateausurface. At that point, the BLCs are transformed into the form ofdried solid crusts (Fig.1) and able to prevent or reduce the release ofdust trapped in the preceding seasons. Thus, extensive BLC devel-opment accounts for loess accumulation and preservation duringglacial phases, and accounts for the formation of thick sequences oflast glacial loess, just as conditions would otherwise becomeunfavourable for deposition and preservation.

6.2. Grain size composition

In previous loess studies, the grain size composition of loessdeposits was interpreted as a consequence of dominant atmo-spheric circulation patterns, wind strength and distance fromsource area (Vandenberghe et al., 1997; Lu et al., 1999; Sun et al.,2004; Prins et al., 2007; Bokhorst et al., 2011). Some recentstudies (Smalley et al., 2011) indicate that BLC and their stickypolysaccharide sheets can also play an important role in deter-mining the grain size composition of loess, by trapping grains ofa certain size. Airborne dust particles have been shown to beselectively incorporated into sediments below crusted surfacesbecause their size is compatible with the eco-physiological needs ofcrustal microorganisms (Belnap, 2001). Furthermore, Williams andEldridge (2011) reported that deposition of sand over a cyano-bacterial soil crust increases nitrogen bioavailability in a semi-aridwoodland environment. If this can be extended to BLC, they can beregarded as a filter for different grain size fractions using silty andsandy material for different segments of their life strategies.

6.3. Structure and loessification

Furthermore, BLC development is often strongly associated withnon-biological (physical) crusts such as rain-induced, erosional anddeposition crusts or chemical crusts (Valentin and Bresson, 1992),with a strong relationship between diversity and soils with a highersilt-clay fraction (Büdel et al., 2009) Development of clay and Cabonds similar to BLC transformation from dry to wet phases fullydepend of climatic seasonality. These independent processes in

some cases can be simultaneous and connected. For example,secondary carbonate nanofibers can fill inter-cellular or space ofpreviously occupied by death cyanobacteria or other microorgan-isms in BLC (e.g. Xu and Chen, 2008).

6.4. Biomarkers and the role(s) of cyanobacteria

The use of cyanobacterial pigments as palaeoenvironmentalbiomarkers noted above holds great promise for elucidatingcomplex relationships between climate, soil formation andconcurrent ecological conditions. The use of these biomarkers willlead to a greater understanding of the extant taxa at given points intime, and in turn, of local/regional palaeoenvironmental conditionsand their shifts. Further, they are usually well preserved over thetimeframe of Quaternary loess deposition. When combined withinformation on palaeoclimate from other proxies, this can providecrucial insight into the relationships between prevailing climateand ecosystem conditions.

The BLOCDUST model presented here involves a central role ofcyanobacteria as colonisers of pristine and (initially) unstable surfaceenvironments. Themodel is supported by the recentfindings of Chenet al. (2012) that, whilst photosynthesis decreases, extracellularpolysaccharide production by the crust-forming cyanobacteriumPhormidium tenue is increased under conditions of low humidity. Inview of the diversity of form, physiological activity and of bioactiveproduct formation in cyanobacteria, it is possible that further attri-butes of cyanobacteria may be involved. For example, as in aquaticenvironments, cyanobacteria in desert crusts produce multipletoxins (cyanotoxins) (Cox et al., 2009; Metcalf et al., 2012). Cyano-toxins have diverse actions including deterrent and toxic effects onother biota, e.g. protozoa (Purdie et al., 2009) which graze uponcyanobacteria. Whether cyanobacteria from loess produce cyano-toxins and whether the latter may contribute to the success of thecyanobacteria in loess formation processes requires investigation.

7. Conclusions

Natural surfaces covered with crust-forming organisms arenamed as biological crusted surfaces (BCS). Biological Loess Crusts(BLC), as one BCS type, are relatively common in modern loessregions and comprise abundant cyanobacterial communities, withlife strategies interlinked with loess plateau processes. Observa-tions and analysis of indicative cyanobacterial pigments suggest therole of their glacial-age analogues in the process of loess formationin arid and semi-arid environmental regions appears to be under-estimated. BLC have a very important role in the capturing, grainsize selection, accumulation (during wet melt phases) and preser-vation (during dry phases) of dust forming loess. BLC may also havea role to play in the development of typical open porous structuresin loess, through loessification. All these outcomes are driven by thelife strategies of cyanobacterial crustal communities, as adaptionsto water stress, protection from harmful UV radiation, and nutrientdeficiency. Furthermore, these preliminary results indicate thatsome cyanobacterial pigments could be regarded as potential BLCbiomarkers, which could be used in turn to constrain the biologicalimpact on the process of loess formation, and the relationshipsbetween climate, BLC and loess accumulation.

Acknowledgements

We thank Mladjen Jovanovi�c for his help during the field work.This research was supported by Project 176020 of the SerbianMinistry of Education and Science.

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