Plant and Soil

, Volume 429, Issue 1–2, pp 213–225 | Cite as

Maximizing establishment and survivorship of field-collected and greenhouse-cultivated biocrusts in a semi-cold desert

  • Anita AntoninkaEmail author
  • Matthew A. Bowker
  • Peter Chuckran
  • Nichole N. Barger
  • Sasha Reed
  • Jayne Belnap
Regular Article



Biological soil crusts (biocrusts) are soil-surface communities in drylands, dominated by cyanobacteria, mosses, and lichens. They provide key ecosystem functions by increasing soil stability and influencing soil hydrologic, nutrient, and carbon cycles. Because of this, methods to reestablish biocrusts in damaged drylands are needed. Here we test the reintroduction of field-collected vs. greenhouse-cultured biocrusts for rehabilitation.


We collected biocrusts for 1) direct reapplication, and 2) artificial cultivation under varying hydration regimes. We added field-collected and cultivated biocrusts (with and without hardening treatments) to bare field plots and monitored establishment.


Both field-collected and cultivated cyanobacteria increased cover dramatically during the experimental period. Cultivated biocrusts established more rapidly than field-collected biocrusts, attaining ~82% cover in only one year, but addition of field-collected biocrusts led to higher species richness, biomass (as assessed by chlorophyll a) and level of development. Mosses and lichens did not establish well in either case, but late successional cover was affected by hardening and culture conditions.


This study provides further evidence that it is possible to culture biocrust components from later successional materials and reestablish cultured organisms in the field. However, more research is needed into effective reclamation techniques.


Biological soil crust Drylands Hardening Field establishment Ecological restoration Ecological rehabilitation Soil erosion resistance 



Level of biocrust development


Utah Test and Training Range



This work was partially supported by the Strategic Environmental Research and Development Program (Grant number RC- 2329; Department of Defense, Department of Energy, and Environmental Protection Agency). We also gratefully acknowledge facilitation of field site permitting and access at the Utah Test and Training Site by Russell Lawrence. We appreciate the help with field collections, greenhouse cultivation, preparation and field data collection by Akasha Faist, Dustin Kebble, Channing Laturno and Brook Stamper. We are also grateful for additional review provided by Akasha Faist, Kara Gibson and two anonymous reviewers that greatly improved the manuscript. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Supplementary material

11104_2017_3300_MOESM1_ESM.docx (223 kb)
ESM 1 (DOCX 222 kb)


  1. Antoninka AJ, Bowker MA, Reed SC, Doherty K (2015) Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor Ecol 24:324–335CrossRefGoogle Scholar
  2. Ayuso Velasco S, Giraldo Silva A, Nelson CJ, Barger NN, Garcia-Pichel F (2016) Microbial nursery production of high-quality biological soil crust biomass for restoration of degraded dryland soils. Appl Environ Microbiol. doi: 10.1128/AEM.02179-16
  3. Barger NN, Belnap J, Ojima DS, Mosier A (2005) NO gas loss from biologically crusted soils in Canyonlands National Park, Utah. Biogeochemistry 75:373–391CrossRefGoogle Scholar
  4. Barger NN, Castle SC, Dean GN (2013) Denitrification from nitrogen-fixing biologically crusted soils in a cool desert environment, southeast Utah, USA. Ecol Process 2:16–22CrossRefGoogle Scholar
  5. Belnap J (1993) Recovery rates of cryptobiotic crusts: inoculant use and assessment methods. Great Basin Nat 53:89–95Google Scholar
  6. Belnap J, Eldridge, D, (2003) Disturbance and recovery of biological soil crusts. In: Belnap J, Lange OL (eds) Biological Soil Crusts: Structure, Function, and Management, Springer-Verlag, Berlin, pp 363-383Google Scholar
  7. Belnap J, Lange OL (2003) Biological Soil Crusts: Structure, Function, and Management. Springer Verlag; Berlin Google Scholar
  8. Belnap J, Phillips S, Troxler T (2006) Soil lichen and moss cover and species richness can be highly dynamic: the effects of invasion by the annual exotic grass Bromus tectorum, precipitation, and temperature on biological soil crusts in SE Utah. Appl Soil Ecol 32:63–76CrossRefGoogle Scholar
  9. Belnap J, Phillips SL, Witwicki DL, Miller ME (2008) Visually assessing the level of development and soils surface stability of cyanobacterially dominated biological soil crusts. Jour Arid Enivoron 72:1257–1264CrossRefGoogle Scholar
  10. Belnap J, Weber B, Büdel B (2016) Biocrusts as an organizing principle in drylands. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Ecological Studies Series. Springer-Verlag, Berlin, pp 3–14CrossRefGoogle Scholar
  11. Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23CrossRefGoogle Scholar
  12. Bowker MA, Antoninka AJ (2016) Rapid ex situ culture of N-fixing soil lichens and biocrusts is enhanced by complementarity. Plant Soil 408:415–428CrossRefGoogle Scholar
  13. Bowker MA, Maestre FT, Escolar C (2010) Biological soil crusts as a model system for examining the diversity-ecosystem function relationship in soils. Soil Biol Biochem 42:405–417CrossRefGoogle Scholar
  14. Bu C, Wu S, Zheng M (2014) Identification of factors influencing restoration of cyanobacteria-dominated biological soil crusts. PLoS One. doi: 10.1371/journal.pone.0090049
  15. Castle SC, Morrison CD, Barger NN (2011) Extraction of chlorophyll a from biological soil crust: a comparison of solvents for spectrophotometric determination. Soil Biol Biochem 43:853–856CrossRefGoogle Scholar
  16. Chaudhary VB, Bowker MA, O’Dell TE, Grace JB, Redman AE, Rillig MC, Johnson NC (2009) Untangling the biological contributions to soil stability in semiarid shrublands. Ecol Appl 19:110–122CrossRefPubMedGoogle Scholar
  17. Chen YQ, Zhao YG, Ran MY (2009) Experimental research on artificial culture method of moss crust in hilly loess Plateau region. Acta bot Boreal-Occident sin 29:586–592Google Scholar
  18. Chiquoine LP, Abella SR, Bowker MA (2016) Rapidly restoring biological soil crusts and ecosystem functions in a severely disturbed desert ecosystem. Ecol Appl 26:1260–1272CrossRefPubMedGoogle Scholar
  19. Condon LA, Pyke DA (2016) Filling the interspace- restoring arid land mosses: source populations, organic matter and overwintering govern success. Ecol Evol 0:1–10. doi: 10.1002/ece3.2448 CrossRefGoogle Scholar
  20. Davidson DW, Bowker M, George D, Phillips SL, Belnap J (2002) Treatment effects on performance of N-fixing lichens in disturbed soil crusts of the Colorado Plateau. Ecol Appl 12:1391–1405CrossRefGoogle Scholar
  21. Delgado-Baquerizo M, Maestre FT, Eldridge DJ, Bowker MA, Ochoa V, Gozalo B, Berdugo M, Val J, Singh BK (2016) Biocrust-forming mosses mitigate the negative impacts of increasing aridity on ecosystem multifunctionality in drylands. New Phytol 209:1540–1552. doi: 10.1111/nph.13688 CrossRefPubMedGoogle Scholar
  22. Doherty KD, Antoninka AJ, Bowker MA, Velasco Ayuso S, Johnson NC (2015) A novel approach to cultivate biocrusts for restoration and experimentation. Ecol Restor 33:13–16CrossRefGoogle Scholar
  23. Escolar C, Maestre FT, Martínez I, Bowker MA (2012) Warming reduces the growth and diversity of lichen-dominated biological soil crusts in a semi-arid environment: implications for ecosystem structure and function. Proc R Soc B 367:3087–3099Google Scholar
  24. Faist AM, Herrick JE, Belnap J, Van Zee JW, Barger NN (2017) Biological soil crust and disturbance controls on surface hydrology in a semi-arid ecosystem. Ecosphere 8(3):e01691CrossRefGoogle Scholar
  25. Ferrenberg S, Reed SC, Belnap J (2015) Climate change and physical disturbance cause similar community shifts in biological soil crusts. Proc Nat Acad Science 112:12116–12121CrossRefGoogle Scholar
  26. Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9:791–802. doi: 10.1038/nrmicro2649 CrossRefPubMedGoogle Scholar
  27. Garcia-Pichel F, Pringault O (2016) Microbiology: cyanobacteria track water in desert soils. Nature 413:380–381CrossRefGoogle Scholar
  28. Grote EE, Belnap J, Housman DC, Sparks JP (2010) Carbon exchange in biological soil crust communities under different temperatures and soil water contents: implications for global change. Glob Chang Biol 16:2763–2774CrossRefGoogle Scholar
  29. Herrick JE, Whitford WG, de Soyza AG, Van Zee JW, Havstad KM, Seybold CA, Walton M (2001) Field soil aggregate stability kit for soil quality and rangeland health evaluations. Catena 44:27–35CrossRefGoogle Scholar
  30. Housman DC, Powers HH, Collins AD, Belnap J (2006) Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan desert. J Arid Environ 66:620–634CrossRefGoogle Scholar
  31. Jonasson S (1983) The point intercept method for non-destructive estimation of biomass. Phytocoenologia 11:385–388CrossRefGoogle Scholar
  32. Lan S, Zhang Q, Wu L, Liu Y, Zhang D, Hu C (2013) Artificially accelerating the reversal of desertification; cyanobacterial inoculation facilitates the success of vegetation communities. Environ Sci Technol 48:307–315CrossRefPubMedGoogle Scholar
  33. Maestre FT, Martın N, Díez B, López-Poma R, Santos F, Luque I, Cortina J (2006) Watering, fertilization, and slurry inoculation promote recovery of biological crust function in degraded soils. Microb Ecol 52:365–377CrossRefPubMedGoogle Scholar
  34. Miller ME, Bowker MA, Reynolds R, Goldstein H (2012) Post-fire land treatments and wind erosion – lessons from the Milford flat fire. Aeolian Res 7:29–44CrossRefGoogle Scholar
  35. Painter TH, Deems J, Belnap J, Hamlet AF, Landry CC, Udall B (2010) Response of Colorado River runoff to dust radiative forcing in snow. Proc Natl Acad Sci 108:3854–3859Google Scholar
  36. Reynolds JF, Stafford-Smith DM, Lambin E, Turner BL III, Mortimore M, Batterbury SPJ, Downing TE, Dowlatabadi T, Fernandez RJ, Herrick JE, Huber-Sannwald E, Jiang H, Leeman R, Lynam T, Maestre FT, Ayarza M, Walker B (2013) Global desertification: building a science for dryland development. Science 316:847–851CrossRefGoogle Scholar
  37. Rosentreter R, Eldridge DJ, Westberg M, Williams L, Grube M (2016) Structure, composition and function of biocrust lichen communites. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Ecological Studies Series. Springer-Verlag, Berlin, pp 121–138CrossRefGoogle Scholar
  38. Rutherford WA, Painter TH, Ferrenberg S, Belnap J, Okin GS, Flagg C, Reed SC (2017) Albedo feedbacks to future climate via climate change impacts on dryland biocrusts. Sci Rep 7. doi: 10.1038/srep44188
  39. Seppelt RD, Downing AJ, Dean-Coe KK, Zhang Y, Zhang J (2016) Bryophytes within biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Ecological Studies Series. Springer-Verlag, Berlin, pp 101–120CrossRefGoogle Scholar
  40. Stark L, Brinda JC, McLetchie DN, Oliver MJ (2012) Extended periods of hydration do not elicit dehardening to desiccation-tolerance in regeneration trails of the moss Syntrichia caninervis. Int J Plant Sci 173:333–343CrossRefGoogle Scholar
  41. USDI BLM, United States Department of Interior, Bureau of Land Management (2007) Burned area emergency stabilization and rehabilitation hand-book. BLM Handbook H-1742-1. USDI BLM, Washington, D.CGoogle Scholar
  42. Weber B, Bowker M, Zhang Y, Belnap J (2016) Natural recovery of biological soil crusts after disturbance. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Ecological Studies Series. Springer-Verlag, Berlin, pp 479–498CrossRefGoogle Scholar
  43. Xiao B, Wang QH, Zhao YG et al (2011) Artificial culture of biological soil crusts and its effects on overland flow and infiltration under simulated rainfall. Appl Soil Ecol 48:11–17CrossRefGoogle Scholar
  44. Zhao Y, Bowker MA, Zhang Y, Zaady E (2016) Enhanced recovery of biological soil crusts after disturbance. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Ecological Studies Series. Springer-Verlag, Berlin, pp 499–523CrossRefGoogle Scholar
  45. Wu N, Zhang YM, Downing A (2009) Comparative study of nitrogenase activity in different types of biological soil crusts in the Gurbantunggut Desert, Northwestern China. J Arid Environ 73(9):828-833Google Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.School of ForestryNorthern Arizona UniversityFlagstaffUSA
  2. 2.United States Geological Survey, Southwest Biological Science CenterMoabUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

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