Soil stability, nitrogen and carbon fixation were assessed for eight biological soil crust community types within a Mojave Desert wilderness site. Cyanolichen crust outperformed all other crusts in multi-functionality whereas incipient crust had the poorest performance. A finely divided classification of biological soil crust communities improves estimation of ecosystem function and strengthens the accuracy of landscape-scale assessments

David Lam

Jeffrey R. Johansen

Joel L. Sachs

John U. Regus

Louis S. Santiago

Pietrasiak, Nicole

Regus, John U

Johansen, Jeffrey R

Lam, David

Sachs, Joel L

Santiago, Louis S

eScholarship - University of California

UC RiversideUC Riverside Previously Published WorksTitleBiological soil crust community types differ in key ecological functionsPermalinkhttps://escholarship.org/uc/item/2cs0f55wAuthorsPietrasiak, NicoleRegus, John UJohansen, Jeffrey Ret al.Publication Date2013-10-01DOI10.1016/j.soilbio.2013.05.011 Peer reviewedeScholarship.org Powered by the California Digital LibraryUniversity of Californiaat SciVerse ScienceDirectSoil Biology & Biochemistry 65 (2013) 168e171Contents lists availableSoil Biology & Biochemistryjournal homepage: www.elsevier .com/locate/soi lbioShort communicationBiological soil crust community types differ in key ecological functionsNicole Pietrasiak a,*, John U. Regus b, Jeffrey R. Johansen c,e, David Lam a, Joel L. Sachs b,Louis S. Santiago daUniversity of California, Riverside, Soil and Water Sciences Program, Department of Environmental Sciences, 2258 Geology Building,Riverside, CA 92521, USAbUniversity of California, Riverside, Department of Biology, University of California, Riverside, CA 92521, USAcBiology Department, John Carroll University, 1 John Carroll Blvd., University Heights, OH 44118, USAdUniversity of California, Riverside, Botany & Plant Sciences Department, 3113 Bachelor Hall, Riverside, CA 92521, USAeDepartment of Botany, Faculty of Science, University of South Bohemia, Branisovska 31, 370 05 Ceske Budejovice, Czech Republica r t i c l e i n f oArticle history:Received 22 February 2013Received in revised form17 May 2013Accepted 18 May 2013Available online 7 June 2013Keywords:Biological soil crustMojave DesertNitrogen fixationCarbon fixationSoil stability* Corresponding author. Present address: Biology Dversity, 1 John Carroll Blvd., University Heights, OH3077; fax: þ1 216 397 4482.E-mail addresses: npiet001@ucr.edu, npietrasijohn.regus@ucr.edu (J.U. Regus), johansen@jcu.eduucr.edu (D. Lam), joels@ucr.edu (J.L. Sachs), santiago@0038-0717/$ e see front matter  2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.soilbio.2013.05.011a b s t r a c tSoil stability, nitrogen and carbon fixation were assessed for eight biological soil crust community typeswithin a Mojave Desert wilderness site. Cyanolichen crust outperformed all other crusts in multi-functionality whereas incipient crust had the poorest performance. A finely divided classification ofbiological soil crust communities improves estimation of ecosystem function and strengthens theaccuracy of landscape-scale assessments. 2013 Elsevier Ltd. All rights reserved.Biological soil crusts carry out essential ecological roles in desertecosystems (Evans and Johansen, 1999; Belnap et al., 2003). How-ever, soil crust community types differ in the degree to which theycontribute to ecosystem functions (Belnap, 2002; Housman et al.,2006; Strauss et al., 2012). In past studies, crust community typeswere often simplistically characterized (e.g. light vs. dark, moss vs.lichen). This resulted in difficulties for cross-investigator or cross-regional comparisons. More importantly, simplistic categoriesmask functional differences in crust types contributing to errors inestimates of ecosystem function. Consequently, ecologists needto refine classifications for crust communities and determineecosystem function.The Mojave Desert is rich in crust communities (Pietrasiak et al.,2011a, 2011b; Pietrasiak, 2012) compared to community types re-ported from other deserts (Pietrasiak, 2012). This study classifiesten biological soil crust community types in the Mojave Desertepartment, John Carroll Uni-44118, USA. Tel.: þ1 216 397ak@jcu.edu (N. Pietrasiak),(J.R. Johansen), dlam010@ucr.edu (L.S. Santiago).All rights reserved.(Table 1) and evaluates three ecosystem functions: carbon fixation,nitrogen fixation, and soil aggregate stability for eight of thesecommunity types.Our study area is within the Mojave Desert physiographicprovince (ca. 35.50 N, 115.68 W). The climate is arid, with a meanannual precipitation of 145 mm and a mean annual temperature of17 C (Turk, 2012). Annual rain events are variable and bimodal(Osborn, 1983). Soil parent material is Mesozoic dolomite alluvium.The vegetation is dominated by Larrea tridentata and Ambrosiadumosa. Within a 2 km2 area, ten crust community types wereidentified (Table 1), with eight prevalent enough for study. Fivereplicates per crust type were sampled in the field to conduct thefield stability test following Herrick et al. (2001). Ten replicates percrust type were collected for laboratory studies of nitrogen andcarbon fixation (Fig. 1).Nitrogen fixation varied significantly (p < 0.0001) among crusttypes (Fig. 1A). Incorporation of 15N into crust ranged from belowdetection to over 100 mmol N2 m2 h1. Cyanolichen crusts hadsignificantly higher nitrogen fixation rates than all other crusttypes. Hairy moss, darkened moss, and green algal lichen crustsalso showed relatively high fixation rates. Two trends were alsonotable. First, fixation rates were very consistent within crustcommunity type (Fig. 1A). Second, untransformed data varied byTable 1Descriptions of the ten biological soil crust communities identified in theMojave Desert based uponmorphology and dominant taxonomic group as visible in the field with thenaked eye, or in some cases, a hand lens. These crust community types are found throughout the arid west and include all types we have observed except the liverwort-dominated crusts found in the coastal sage-scrub.Crust typecodeCrust typeidentificationDescriptionIC Incipient algal/fungalcrustWeakly consolidated, soft crust that breaks apart easily but displays fungal hyphae or cyanobacterial filaments, dominantcomponents are fungi and/or non-heterocytous cyanobacteria (Microcoleus spp., Leptolyngbya spp.); ubiquitousFC Fungal crust Embedded underneath shrub litter or a sand layer in the open, fungal hyphae clearly visible, dominant components are fungiLAC Light algal crust Inconspicuous colored crust dominantly composed of cyanobacteria (mostly Microcoleus spp. and Pseudanabaenaceae spp.) andeukaryotic algae (e.g. Bracteacoccus, Chlorosarcinopsis, Scenedesmus, Chlorella); ubiquitousDAC Dark algal crust Dark-colored crust dominantly composed of cyanobacteria (colored by surface-growing heterocytous taxa in Nostoc, Scytonema,and Hassallia); present but too rare for study in our site, commonly found on granitic soils elsewhere in the Mojave DesertCLC Cyanolichen crust Lichens that have cyanobacterial photobionts, e.g. Collema; broadly distributed in intershrub spacesGLC Green algal lichen crust Lichens that have green algal photobionts, e.g. Placidium; broadly distributed in intershrub spacesSMC Smooth moss crust Moss crust with small phyllids on short thalli, e.g. Bryum; present but too rare for study in our site, commonly found on graniticsoils elsewhere in the Mojave DesertRMC Rough moss crust Moss crust with minor hair-like extensions on phyllids, brownish when dry, green to brown-green when moist, e.g. Syntrichia;broadly distributed in intershrub spacesHMC Hairy moss crust Moss crust with extensive hair-like extensions on phyllids that appear like whitish-gray carpets, e.g. Crossidium, Pterygoneurum;requiring shady environmentsDMC Dark moss crust Clearly blackened, moss-dominated crust (mostly Syntrichia), associated with heterocytous cyanobacteria (Nostoc spp.); broadlydistributed in intershrub spacesCA BFig. 1. Boxplots calculated in R (R Core Team, 2012) showing the three ecosystem functions investigated among eight biological soil crust community types. Dark bars representmedian values, with boxes enclosing the upper and lower inner quartiles, with extremes indicated by whiskers or circles when the extreme is an outlier (Crawley, 2007), black “x”represent means of log-transformed data. Lowercase letters represent significant differences in means (stability) or means of log-transformed data (N-fixation, C-fixation) detectedwith ANOVA and the LSD test. For key to crust community types see Table 1. Field collection of dry soil crusts from randomly selected sites occurred over one weekend in April 2011;samples were refrigerated until analysis, which occurred within 30 days. (A) Nitrogen fixation as determined using fixation of 15N enriched gas following methods of Pietrasiak(2012). Briefly, rates were determined following a 24-h rehydration period at field capacity, and a 48-h incubation period, with rates calculated according to Warembourg(1992); (B) carbon fixation as determined following hydration at field capacity from a 2-h incubation period at a photosynthetic photon flux density of 1600 mmol m2 s1 atambient relative humidity and temperature; (C) Herrick’s stability index values.N. Pietrasiak et al. / Soil Biology & Biochemistry 65 (2013) 168e171 169N. Pietrasiak et al. / Soil Biology & Biochemistry 65 (2013) 168e171170five orders of magnitude between fungal crust (lowest) and thecyanolichen crust (highest). If cyanolichen crusts are abundant,they can potentially be the dominant crust-associated nitrogenfixers in desert ecosystems.Carbon fixation also varied significantly (p < 0.0001) amongcrust types (Fig. 1B). Cyanolichen crust had the highest fixationrates, but did not differ significantly from darkened moss crust.Light algal crust, incipient algal-fungal crust, and fungal crustshowed substantially lower fixation rates than crusts containingmoss and/or lichen species (Fig. 1B).The stability test demonstrated that most crust types had themaximal stability possible with this metric (Fig. 1C). Light algalcrust was significantly less stable, but incipient algal-fungal crustwas significantly the least stable among all crust types.This study showed that careful categorization of crust commu-nity types can lead tomore accurate assessments of their ecologicalsignificance. If we had used amore simplistic measure, such as lightand dark crust, or moss and lichen crusts, we would have missedthe pattern of variation that became clear with the more finelydivided classification. The different moss crusts showed minimalvariation in ecosystem function. It would be practical to combinethese community types. Given the ease with which they can berecognized in the field, the finer classification seems justified. Thegreen algal lichen and cyanolichen crusts were significantlydifferent in both nitrogen and carbon fixation, and future studiesshould distinguish between these communities. Dark algal crustand smooth moss crusts were present in the study site, but so rarethat it was not feasible to include them in this study (Table 1).Overall, lichen and moss crusts performed best in all ecologicalfunctions. The cyanolichen crust, dominated by Collema tenax andCollema coccophorum, clearly had the highest fixation rates for bothcarbon and nitrogen. This finding is in agreement with the results ofothers (Lange et al., 1998; Belnap, 2002; Lange, 2003). High fixationrates may be supported by the carbon concentrating mechanism(Badger et al., 1993), the high nitrogen fixation capacity of the cya-nobacterial symbiont (Lange et al., 1998), and prolonged waterholding capacity (Lange et al., 1998). Thus, landscapes that support asubstantial ground cover of these cyanolichens may have enhancedfertility in termsof nitrogen andcarbon. Green algal lichen crusts hadobservable cyanobacterial colonies growing among lichen squa-mules, but did not show comparably high nitrogen fixation rates.Mosses do not fix nitrogen, but are often associated withnitrogen-fixing cyanobacteria (Wu et al., 2009; Zhao et al., 2010).Examination of Clark Mountain hairy moss crusts revealed smallcolonies of lichenized and free-living cyanobacteria (i.e. Nostoc)growing on the soil as well as on the phyllids, and these cyano-bacteria are likely responsible for the elevated nitrogen fixation ofthese crusts.Light algal crusts were low in both nitrogen and carbon fixation.These crusts are devoid of heterocytous cyanobacteria (Garcia-Pichel and Belnap, 1996; Belnap, 2002; Garcia-Pichel et al., 2003).Typically, the dominant community components in these crusts arefilamentous non-heterocytous cyanobacteria such as Microcoleusand Leptolyngbya species. Minor nitrogen fixation may occurthrough heterotrophic fixation of symbiotic bacteria living in thesheath material of these filamentous cyanobacteria (Steppe et al.,1996) or due to sparse free-living heterocytous cyanobacteria(Garcia-Pichel and Belnap, 1996).Fungal crusts at the Clark Mountains mostly formed underneaththe litter layer adjacent to shrubs (especially with L. tridentata).These crusts generally lack cyanobacteria and are associated with arich heterotrophic microbial community as well as an evidentcoccoid green algal assemblage. In contrast to the study by Zaadyet al. (1998), heterotrophic nitrogen fixation was minimal infungal crusts from our study site.This is the first instance in which different crust communitytypes have been compared based on their stability index values.Previous studies using Herrick’s stability test focused instead on therelationships between soil aggregate stability and total crust cover,or reported mean values of mixed community crusts (Bowker et al.,2008; Chaudhary et al., 2009; Carpenter and Chong, 2010; Herricket al., 2010). In our study, only incipient crusts showed depressedstability values. These findings indicate that all crusts contribute tostability even if they do not play significant roles in nitrogen andcarbon fixation. Thus, prevention of erosion due to water and windrepresents the major ecosystem function that is common to allcrust types.In conclusion, if a finely divided classification systemwere used,much greater precision and accuracy would be possible whenestimating fixation rates and importance of crust community typesat the landscape scale.AcknowledgmentsJoy Matthews assisted with protocol development for the 15Nenrichment study. Exequiel Ezcurra provided the 15N for theexperiment.ReferencesBadger, M.R., Pfanz, H., Büdel, B., Heber, U., Lange, O., 1993. Evidence for the func-tioning of photosynthetic CO2-concentrating mechanisms in lichens containinggreen algal and cyanobacterial photobionts. Planta 191, 57e70.Belnap, J., 2002. Nitrogen fixation in biological soil crusts from southeast Utah, USA.Biology and Fertility of Soils 35, 128e135.Belnap, J., Büdel, B., Lange, O.L., 2003. Biological soil crust: characteristics and dis-tribution. In: Belnap, J., Lange, O.L. 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Biological soil crust community types differ in key ecological functions

Biological soil crust community types differ in key ecological functions

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