Plant and Soil

, Volume 366, Issue 1–2, pp 35–47 | Cite as

Biological soil crusts increase the resistance of soil nitrogen dynamics to changes in temperatures in a semi-arid ecosystem

  • Manuel Delgado-Baquerizo
  • Fernando T. Maestre
  • Antonio Gallardo
Regular Article



Biological soil crusts (BSCs), composed of mosses, lichens, liverworts and cyanobacteria, are a key component of arid and semi-arid ecosystems worldwide, and play key roles modulating several aspects of the nitrogen (N) cycle, such as N fixation and mineralization. While the performance of its constituent organisms largely depends on moisture and rainfall conditions, the influence of these environmental factors on N transformations under BSC soils has not been evaluated before.


The study was done using soils collected from areas devoid of vascular plants with and without lichen-dominated BSCs from a semi-arid Stipa tenacissima grassland. Soil samples were incubated under different temperature (T) and soil water content (SWC) conditions, and changes in microbial biomass-N, dissolved organic nitrogen (DON), amino acids, ammonium, nitrate and both inorganic N were monitored. To evaluate how BSCs modulate the resistance of the soil to changes in T and SWC, we estimated the Orwin and Wardle Resistance index.


The different variables studied were more affected by changes in T than by variations in SWC at both BSC-dominated and bare ground soils. However, under BSCs, a change in the dominance of N processes from a net nitrification to a net ammonification was observed at the highest SWC, regardless of T.


Our results suggest that the N cycle is more resistant to changes in T in BSC-dominated than in bare ground areas. They also indicate that BSCs could play a key role in minimizing the likely impacts of climate change on the dynamics of N in semi-arid environments, given the prevalence and cover of these organisms worldwide.


Semiarid ecosystem N depolymerization rate N mineralization rate DON 



We thank the Instituto Madrileño de Investigación y Desarrollo Rural, Agrario y Alimentario (IMIDRA) for allowing us to work in the Aranjuez Experimental Station (Finca de Sotomayor), J. Durán, A. Rodríguez and two reviewers for their helpful comments and suggestions on previous versions of this manuscript. This research is supported by the European Research Council (ERC) under the European Community’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant agreement n° 242658 (BIOCOM) and by the Ministry of Science and Innovation of the Spanish Government, Grant nº CGL2010-21381. FTM acknowledges support from the Spanish Ministerio de Educación (“Salvador de Madariaga program”, PR2010-0230) during the writing of the manuscript.

Supplementary material

11104_2012_1404_MOESM1_ESM.doc (113 kb)
ESM 1 (DOC 113 kb)
11104_2012_1404_MOESM2_ESM.doc (171 kb)
ESM 2 (DOC 171 kb)


  1. Almagro M, Querejeta JI, Martınez-Mena M (2009) Temperature dependence of soil CO2 efflux is strongly modulated by seasonal patterns of moisture availability in a Mediterranean ecosystem. Soil Biol Biochem 41:594–605CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235PubMedCrossRefGoogle Scholar
  4. 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
  5. Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fertil Soils 35:128–135CrossRefGoogle Scholar
  6. Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 3178:3159–3178CrossRefGoogle Scholar
  7. Belnap J, Lange OL (2003) Biological soil crusts: structure, function, and management. Springer, Berlin, New York, pp 3–30CrossRefGoogle Scholar
  8. Belnap J, Phillips SL, Flint S, Money J, Caldwell M (2008) Global change and biological soil crusts: effects of ultraviolet augmentation under altered precipitation regimes and nitrogen additions. Glob Chang Biol 14:670–686CrossRefGoogle Scholar
  9. Ben-David EA, Zaady E, Sher Y, Nejidat A (2011) Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses. FEMS Microbiol Ecol 76:492–503Google Scholar
  10. Bregliani MM, Ros GH, Temminghoff EJM, Van Riemsdijk WH (2010) Nitrogen mineralization in soils related to initial extractable organic nitrogen: effect of temperature and time. Comm Soil Sci Plant Anal 41(11):1383–1398CrossRefGoogle Scholar
  11. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method tomeasure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842CrossRefGoogle Scholar
  12. Castillo-Monroy AP, Delgado-Baquerizo M, Maestre FT, Gallardo A (2010) Biological soil crusts modulate nitrogen availability in semi-arid ecosystems: insights from a Mediterranean grassland. Plant Soil 333:21–34CrossRefGoogle Scholar
  13. Castillo-Monroy AP, Maestre FT, Rey A, Soliveres S, García-Palacios P (2011a) Biological soil crust microsites are the main contributor to soil respiration in a semiarid ecosystem. Ecosystems 14:835–847CrossRefGoogle Scholar
  14. Castillo-Monroy AP, Bowker MA, Maestre FT, Rodr S, Martinez I, Barraza-Zepeda CE (2011b) Relationships between biological soil crusts, bacterial diversity and abundance, and ecosystem functioning: insights from a semi-arid Mediterranean environment. J Veg Sci 22:165–174CrossRefGoogle Scholar
  15. Chantigny MH, Angers DA, Kaiser K, Kalbitz K (2006) Extraction and characterization of dissolved organic matter. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis, Canadian soil of society science, pp 617–635Google Scholar
  16. Cui M, Caldwell MM (1997) A large ephemeral release of nitrogen upon wetting of dry soil and corresponding root responses in the field. Plant Soil 191:291–299CrossRefGoogle Scholar
  17. Delgado-Baquerizo M, Gallardo A (2011) Depolymerization and mineralization rates at 12 Mediterranean sites with varying soil N availability. A test for the Schimel and Bennett model. Soil Biol Biochem 43:693–696CrossRefGoogle Scholar
  18. Delgado-Baquerizo M, Castillo-Monroy AP, Maestre FT, Gallardo A (2010) Change in the dominance of N forms within a semi-arid ecosystem. Soil Biol Biochem 42:376–378CrossRefGoogle Scholar
  19. Delgado-Baquerizo M, Covelo F, Gallardo A (2011) Dissolved organic nitrogen in Mediterranean ecosystems. Pedosphere 21:309–318CrossRefGoogle Scholar
  20. Del Prado R, Sancho LG (2007) Dew as a key factor for the distribution pattern of the lichen species Teloschistes lacunosus in the Tabernas Desert (Spain). Flora 202:417–428Google Scholar
  21. Fernandez DP, Neff JC, Belnap J, Reynolds RL (2006) Soil respiration in the cold desert environment of the Colorado Plateau (USA): abiotic regulators and thresholds. Biogeochemistry 78:247–265CrossRefGoogle Scholar
  22. Finzi AC, Austin AT, Cleland EE, Serita D, Frey SD, Houlton BZ, Wallenstein MD (2011) Coupled biochemical cycles: responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Front Ecol Environ 9:61–67CrossRefGoogle Scholar
  23. Gallardo A, Schlesinger WH (1993) Carbon and nitrogen limitations of soil microbial biomass in desert ecosystems. Biogeochemistry 18:1–17CrossRefGoogle Scholar
  24. Gallardo A, Schlesinger WH (1995) Factors determining soil microbial biomass and nutrient immobilization in desert soils. Biogeochemistry 28:55–68CrossRefGoogle Scholar
  25. Gallardo A, Merino J (1998) Soil nitrogen dynamics in response to carbon increase in a Mediterranean Shrubland of SW Spain. Soil Biol Biochem 30:1349–1358CrossRefGoogle Scholar
  26. Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sinauer Associates, SunderlandGoogle Scholar
  27. Grote EE, Belnap J, Housman DC, Sparks JP (2010) Carbon exchange in biological soil crust communities under differential temperatures and soil water content: implications for global change. Glob Chang Biol 16:2763–2774CrossRefGoogle Scholar
  28. Gundlapally SR, García-Pichel F (2006) The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol 52:345–357PubMedCrossRefGoogle Scholar
  29. Housman DC, Yeager CM, Darby BJ, Sanford Jr RL, Kuske CR, Neher DA, Belnap J (2007) Heterogeneity of soil nutrients and subsurface biota in a dryland ecosystem. Soil Biol Biochem 39:2138–2149Google Scholar
  30. IPCC (2007) Climate Change 2007: synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. In: Core Writing Team, Pachauri RK, Reisinger A (eds). IPCC, Geneva, Switzerland, p 104Google Scholar
  31. Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999CrossRefGoogle Scholar
  32. Kladivko EJ, Keeney DR (1987) Soil nitrogen mineralization as affected by water and temperature interactions. Biol Fertil Soils 5:248–252CrossRefGoogle Scholar
  33. Korner C (2000) Biosphere responses to CO2 enrichment. Ecol Appl 10:1590–1619Google Scholar
  34. Lange OL (2003) Photosynthesis of soil-crust biota as dependent on environmental factors. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, New York, pp 217–240Google Scholar
  35. Maestre FT, Bautista S, Cortina J, Díaz G, Honrubia M, Vallejo VR (2002) Microsite and mycorrhizal inoculum effects on the establishment of Quercus coccifera in a semi-arid degraded steppe. Ecol Eng 19:289–295CrossRefGoogle Scholar
  36. Maestre FT, Martín 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 52:365–377PubMedCrossRefGoogle Scholar
  37. Maestre FT, Bowker MA, Puche MD, Hinojosa MB, Martínez I, García-Palacios P, Castillo AP, Soliveres S, Luzuriaga AL, Sánchez AM, Carreira JA, Gallardo A, Escudero A (2009) Shrub encroachment can reverse desertification in Mediterranean semiarid grasslands. Ecol Lett 12:930–941PubMedCrossRefGoogle Scholar
  38. Maestre FT, Bowker MA, Puche MD, Escolar C, Soliveres S, Mouro S, García-Palacios P, Castillo-Monroy AP, Martínez I, Escudero A (2010) Do biotic interactions modulate ecosystem functioning along abiotic stress gradients? Insights from semi-arid plant and biological soil crust communities. Phil Trans R Soc B 365:2057–2070PubMedCrossRefGoogle Scholar
  39. Maestre FT, Bowker MA, Cantón Y, Castillo-Monroy AP, Cortina J, Escolar C, Escudero A, Lázaro R, Martínez I (2011) Ecology and functional roles of biological soil crusts in semi-arid ecosystems of Spain. J Arid Environ 75:1282–1291CrossRefGoogle Scholar
  40. Marqués MJ, Bienes R, Pérez-Rodríguez R, Jiménez L (2008) Soil degradation in Central Spain due to sheet water erosion by low-intensity rainfall events. Earth Surf Proc Land 33:414–423CrossRefGoogle Scholar
  41. Orwin KH, Wardle DA (2004) New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biol Biochem 36:1907–1912CrossRefGoogle Scholar
  42. Reinard JC (2006) Communications research statistics. Sage, Thousand OaksGoogle Scholar
  43. Reynolds JF, Smith DM, Lambin EF, Turner BL, Mortimore M, Batterbury S, Downing TE, Dowlatabadi H, Fernandez RJ, Herrick JE, Huber-Sannwald E, Jiang H, Leemans R, Lynam T, Maestre FT, Ayarza M, Walker B (2007) Global desertification: building a science for dryland development. Science 316:847–851PubMedCrossRefGoogle Scholar
  44. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602CrossRefGoogle Scholar
  45. Schimel DS (2010) Drylands in the earth system. Science 327:418–419PubMedCrossRefGoogle Scholar
  46. Schwinning S, Sala OE (2004) Hierarchy of responses to resource pulses in arid and semi-arid ecosystems. Oecologia 141:211–220PubMedGoogle Scholar
  47. Sims GK, Ellsworth TR, Mulvaney RL (1995) Microscale determination of inorganic nitrogen in water and soil extracts. Commun Soil Sci Plant Anal 26:303–316CrossRefGoogle Scholar
  48. Sollins P, Glassman C, Paul EA, Swantston C, Lajtha K, Heil JW, Ellikott T (1999) Soil carbon and nitrogen: pools and fraction. In: Robertson GP (ed) Standard soil methods for long-term ecological research. Oxford University Press, Oxford, pp 89–105Google Scholar
  49. Soule T, Anderson IJ, Johnson SL, Bates ST, Garcia-pichel F (2009) Archaeal populations in biological soil crusts from arid lands in North America. Soil Biol Biochem 41:2069–2074CrossRefGoogle Scholar
  50. Szukics U, Abell GC, Hodl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S (2010) Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol Ecol 72:395–406PubMedCrossRefGoogle Scholar
  51. USDA (2003) Key to soil taxonomy. Handbook 436, 9th edn. Soil Survey Staff, NRCS, Washington, USA, p 332Google Scholar
  52. Whitford WG (2002) Ecology of desert ecosystems. Academy, New York, p 151Google Scholar
  53. Yeager CM, Kornosky JL, Housman DC, Grote EE, Belnap J, Kuske CR (2004) Diastrophic community structure and function in two succession stages of biological soil crusts from the Colorado plateau and Chihuahuan desert. Appl Environ Microbiol 70:973–983PubMedCrossRefGoogle Scholar
  54. Zornoza R, Mataix-Solera J, Guerrero C, Arcenegui V, Mataix-Beneyto J (2009) Storage effects on biochemical properties of air-dried soil samples from southeastern Spain. Arid Land Res Manag 23:213–222CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Manuel Delgado-Baquerizo
    • 1
  • Fernando T. Maestre
    • 2
  • Antonio Gallardo
    • 1
  1. 1.Departamento de Sistemas Físicos, Químicos y NaturalesUniversidad Pablo de OlavideSevillaSpain
  2. 2.Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Escuela Superior de Ciencias Experimentales y TecnologíaUniversidad Rey Juan CarlosMóstolesSpain

Personalised recommendations