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Biocrusts in the Context of Global Change

  • Sasha C. Reed
  • Fernando T. Maestre
  • Raúl Ochoa-Hueso
  • Cheryl R. Kuske
  • Anthony Darrouzet-Nardi
  • Mel Oliver
  • Brian Darby
  • Leopoldo G. Sancho
  • Robert L. Sinsabaugh
  • Jayne Belnap
Part of the Ecological Studies book series (ECOLSTUD, volume 226)

Abstract

A wide range of studies show global environmental change will profoundly affect the structure, function, and dynamics of terrestrial ecosystems. The research synthesized here underscores that biocrust communities are also likely to respond significantly to global change drivers, with a large potential for modification to their abundance, composition, and function. We examine how elevated atmospheric CO2 concentrations, climate change (increased temperature and altered precipitation), and nitrogen deposition affect biocrusts and the ecosystems they inhabit. We integrate experimental and observational data, as well as physiological, community ecology, and biogeochemical perspectives. Taken together, these data highlight the potential for biocrust organisms to respond dramatically to environmental change and show how changes to biocrust community composition translate into effects on ecosystem function (e.g., carbon and nutrient cycling, soil stability, energy balance). Due to the importance of biocrusts in regulating dryland ecosystem processes and the potential for large modifications to biocrust communities, an improved understanding and predictive capacity regarding biocrust responses to environmental change are of scientific and societal relevance.

Keywords

Vascular Plant Biological Soil Crust Mojave Desert Colorado Plateau Altered Precipitation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

SCR and JB were supported by the USGS Ecosystems Mission Area. A significant portion of the studies of biocrust bacterial communities under warming, altered precipitation, and elevated CO2 conditions described here was supported by the US Department of Energy Office of Science, Office of Biological and Environmental Research Terrestrial Ecosystem Sciences Program grants to JB, CRK, and SCR (e.g., Award Number DE-SC-0008168), and research grants to CRK from the Climate and Environmental and the Biological and System Science Divisions. FTM was supported by the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007–2013)/ERC Grant agreement 242658 (BIOCOM), and LGS was supported by the Spanish grant CTM2012-3822-C01-02 during the writing of this chapter. We are grateful to Burkhard Büdel and Bettina Weber for their insightful comments on previous drafts of this chapter and to E. Geiger, L. Allred, and M. Moats for their help with chapter preparation. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US government.

References

  1. Amthor JS, Hanson PJ, Norby RJ, Wullschleger SD (2010) A comment on “Appropriate experimental ecosystem warming methods by ecosystem, objective, and practicality” by Aronson and McNulty. Agric For Meteorol 150:497–498CrossRefGoogle Scholar
  2. Aronson EL, McNulty SG (2009) Appropriate experimental ecosystem warming methods by ecosystem, objective, and practicality. Agric For Meteorol 149:1791–1799CrossRefGoogle Scholar
  3. Ault TR, Cole JE, Overpeck JT, Pederson GT, Meko DM (2014) Assessing the risk of persistent drought using climate model simulations and paleoclimate data. J Clim 27:7529–7549CrossRefGoogle Scholar
  4. Austin AT, Sala OE, Jackson RB (2006) Inhibition of nitrification alters carbon turnover in the Patagonian steppe. Ecosystems 9:1257–1265CrossRefGoogle Scholar
  5. Ayres A, Wall DH, Simmons BL, Field CB, Milchunas DG, Morgan JA, Roy J (2008) Belowground nematode herbivores are resistant to elevated atmospheric CO2 concentrations in grassland ecosystems. Soil Biol Biochem 40:978–985CrossRefGoogle Scholar
  6. Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ (1999) Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 13:650–660CrossRefGoogle Scholar
  7. Barker DH, Stark LR, Zimpfer JF, Mcletchie ND, Smith SD (2005) Evidence of drought-induced stress on biotic crust moss in the Mojave Desert. Plant Cell Environ 28:939–947CrossRefGoogle Scholar
  8. Belnap J (2002) Nitrogen fixation in biological soil crust from southeast Utah, USA. Biol Fertil Soils 35:128–135CrossRefGoogle Scholar
  9. Belnap J, Gillette DA (1998) Vulnerability of desert biological soil crusts to wind erosion: the influences of crust development, soil texture, and disturbance. J Arid Environ 39:133–142CrossRefGoogle Scholar
  10. Belnap J, Phillips SL, Miller ME (2004) Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia 141:306–316PubMedCrossRefGoogle Scholar
  11. Belnap J, Walker BJ, Munson SM, Gill RA (2014) Controls on sediment production in two U.S. deserts. Aeolian Res 14:15–24CrossRefGoogle Scholar
  12. Berdugo M, Soliveres S, Maestre FT (2014) Vascular plants and biocrusts modulate how abiotic factors affect wetting and drying events in drylands. Ecosystems 17:1242–1256CrossRefGoogle Scholar
  13. Billings SA, Schaeffer SM, Evans RD (2002) Trace N gas losses and N mineralization in Mojave desert soil exposed to elevated CO2. Soil Biol Biochem 34:1777–1784CrossRefGoogle Scholar
  14. Blankinship JC, Niklaus PA, Hungate BA (2011) A meta-analysis of responses of soil biota to global change. Oecologia 165:553–565PubMedCrossRefGoogle Scholar
  15. Blett TF, Lynch JA, Pardo LH, Huber C, Haeuber R, Pouyat R (2014) FOCUS: a pilot study for national-scale critical loads development in the United States. Environ Sci Policy 38:225–236CrossRefGoogle Scholar
  16. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-W, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59PubMedCrossRefGoogle Scholar
  17. Botting RS, Fredeen AL (2006) Net ecosystem CO2 exchange for moss and lichen dominated forest floors of old-growth sub-boreal spruce forests in central British Columbia, Canada. For Ecol Manage 235:240–251CrossRefGoogle Scholar
  18. Bowker MA, Belnap J, Rosentreter R, Graham B (2004) Wildfire-resistant biological soil crusts and fire-induced loss of soil stability in Palouse prairies, USA. Appl Soil Ecol 26:41–52CrossRefGoogle Scholar
  19. Bowker MA, Maestre FT, Escolar C (2010) Biological crusts as a model system for examining the biodiversity–ecosystem function relationship in soils. Soil Biol Biochem 42:405–417CrossRefGoogle Scholar
  20. Bowker MA, Mau RL, Maestre FT, Escolar C, Castillo-Monroy AP (2011) Functional profiles reveal unique roles of various biological soil crust organisms in Spain. Funct Ecol 25:787–795CrossRefGoogle Scholar
  21. Branquinho C, Pinho P, Dias T, Cruz C, Máguas C, Martins-Loução MA (2010) Lichen transplants at our service for measuring atmospheric NH3 deposition. Bibliotheca Lichenologica 105:103–112Google Scholar
  22. Brinda JC, Fernando C, Stark LR (2011) Ecology of bryophytes in Mojave Desert biological soil crusts: effects of elevated CO2 on sex expression, stress tolerance, and productivity in the moss Syntrichia caninervis Mitt. In: Bryophyte ecology and climate change. Cambridge University Press, Cambridge, pp 169–191Google Scholar
  23. Büdel B, Darienko T, Deutschewitz K, Dojani S, Friedl T, Mohr KI, Salisch M, Reisser W, Weber B (2009) Southern African biological soil crusts are ubiquitous and highly diverse in drylands, being restricted by rainfall frequency. Microb Ecol 57:229–247PubMedCrossRefGoogle Scholar
  24. Buitink J, Hoekstra F, Leprince O (2002) Biochemistry and biophysics of tolerance systems. In: Desiccation and survival in plants: drying without dying. CAB International, Wallingford, UK, pp 293–318Google Scholar
  25. Cable JM, Huxman TE (2004) Precipitation pulse size effects on Sonoran Desert soil microbial crusts. Oecologia 141:317–324PubMedCrossRefGoogle Scholar
  26. Cable JM, Ogle K, Williams DG, Weltzin JF, Huxman TE (2008) Soil texture drives responses of soil respiration to precipitation pulses in the Sonoran Desert: implications for climate change. Ecosystems 11:961–979CrossRefGoogle Scholar
  27. Castillo-Monroy AP, Maestre FT (2011) La costra biologica del suelo: avances recientes en el conocimiento de su estructura y funcion ecologica. Revista Chilena de Historia Natural 84:1–21CrossRefGoogle Scholar
  28. Chapin FS III, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277:500–504CrossRefGoogle Scholar
  29. Coe KK, Belnap J, Grote EE, Sparks JP (2012a) Physiological ecology of the desert moss Syntrichia caninervis after ten years exposure to elevated CO2: evidence for enhanced photosynthetic thermotolerance. Physiol Plant 144:346–356PubMedCrossRefGoogle Scholar
  30. Coe KK, Belnap J, Sparks JP (2012b) Precipitation-driven carbon balance controls survivorship of desert biocrust mosses. Ecology 93:1626–1636PubMedCrossRefGoogle Scholar
  31. Dai A (2011a) Characteristics and trends in various forms of the Palmer Drought Severity Index (PDSI) during 1900-2008. J Geophys Res 116:D12Google Scholar
  32. Dai A (2011b) Drought under global warming: a review. WIREs Clim Change 2:45–46CrossRefGoogle Scholar
  33. Dai A (2013) Increasing drought under global warming in observations and models. Nat Clim Change 3:52–58CrossRefGoogle Scholar
  34. Darby BJ, Housman DC, Zaki AM, Shamout Y, Adl SM, Belnap J, Neher DA (2006) Effects of altered temperature and precipitation on desert protozoa associated with biological soil crusts. J Eukaryot Microbiol 53:507–514PubMedCrossRefGoogle Scholar
  35. Darby BJ, Neher DA, Belnap J (2010) Impact of biological soil crusts and desert plants on soil microfaunal community composition. Plant Soil 328:421–431CrossRefGoogle Scholar
  36. Darby BJ, Neher DA, Housman DC, Belnap J (2011) Few apparent short-term effects of elevated soil temperature and increased frequency of summer precipitation on the abundance and taxonomic diversity of desert soil micro- and meso-fauna. Soil Biol Biochem 43:1474–1481CrossRefGoogle Scholar
  37. Darrouzet-Nardi A, Reed SC, Grote EE, Belnap J (2015) Observations of net soil exchange of CO2 in a dryland show experimental warming increases carbon losses in biocrust soils. Biogeochemistry 126:363–378. doi: 10.1007/s10533-015-0163-7
  38. Delgado Baquerizo M, Gallardo A, Covelo F, Prado-Comesana A, Ochoa V, Maestre FT (2015) Differences in the chemistry of thalli determine species-specific effects of biocrust-forming lichens on soil nutrients and microbial communities. Funct Ecol 29(8):1087–1098CrossRefGoogle Scholar
  39. Delgado-Baquerizo M, Maestre FT, Gallardo A, Quero JL, Ochoa V, Garcia-Gomez M, Escolar C, Garcia-Palacios P, Berdugo M, Valencia E, Gozalo B, Noumi Z, Derak M, Wallenstein MD (2013a) Aridity modulates N availability in arid and semiarid Mediterranean grasslands. Plos One 8:e59807PubMedPubMedCentralCrossRefGoogle Scholar
  40. Delgado-Baquerizo M, Morillas L, Maestre FT, Gallardo A (2013b) Biocrusts control the nitrogen dynamics and microbial functional diversity of semi-arid soils in response to nutrient additions. Plant Soil 372:643–654CrossRefGoogle Scholar
  41. Delgado-Baquerizo M, Maestre FT, Escolar C, Gallardo A, Ochoa V, Gozalo B, Prado-Comesaña A (2014) Direct and indirect impacts of climate change on microbial and biocrust communities alter the resistance of N cycle in dryland soils. J Ecol 102:1592–1605CrossRefGoogle Scholar
  42. Dermody O, Weltzin JF, Engel EC, Allen P, Norby RJ (2007) How do elevated [CO2], warming, and reduced precipitation interact to affect soil moisture and LAI in an old field ecosystem? Plant Soil 301:255–266CrossRefGoogle Scholar
  43. Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462CrossRefGoogle Scholar
  44. Escolar C, Martinez I, Bowker MA, Maestre FT (2012) Warming reduces the growth and diversity of biological soil crusts in a semi-arid environment: implications for ecosystem structure and functioning. Philos Trans R Soc B Biol Sci 367:3087–3099CrossRefGoogle Scholar
  45. Felde VJMNL, Peth S, Uteau-Puschmann D, Drahorad S, Felix-Henningsen P (2014) Soil microstructure as an under-explored feature of biological soil crust hydrological properties: case study from the NW Negev Desert. Biodivers Conserv 23:1687–1708CrossRefGoogle Scholar
  46. Feng S, Fu Q (2013) Expansion of global drylands under a warming climate. Atmos Chem Phys 13:10081–10094CrossRefGoogle Scholar
  47. Ferrenberg S, Reed SC, Belnap J (2015) Climate change and physical disturbance cause similar community shifts in biological soil crusts. Proc Natl Acad Sci USA 112:12116–12121PubMedPubMedCentralCrossRefGoogle Scholar
  48. Funk FA, Loydi A, Peter G (2014) Effects of biological soil crusts and drought on emergence and survival of a Patagonian perennial grass in the Monte of Argentina. J Arid Land 6:735–741CrossRefGoogle Scholar
  49. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892PubMedCrossRefGoogle Scholar
  50. Garcia-Pichel F, Loza V, Marusenko Y, Mateo P, Potrafka RM (2013) Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science 340:1574–1577PubMedCrossRefGoogle Scholar
  51. Garfin G, Franco G, Blanco H, Comrie A, Gonzalez P, Piechota T, Smyth R, Waskom R (2014) In: Melillo JM, Richmond TC, Yohe GW (eds) Ch. 20: Southwest. Climate change impacts in the United States: The third national climate assessment. U.S. Global Change Research Program, Washington, DC, pp 462–486Google Scholar
  52. González-Megías A, Menéndez R (2012) Climate change effects on above- and below-ground interactions in a dryland ecosystem. Philos Trans R Soc B Biol Sci 367:3115–3124CrossRefGoogle Scholar
  53. Gross KL, Mittelbach GG, Reynolds HL (2005) Grassland invasibility and diversity: responses to nutrients, seed input, and disturbance. Ecology 86:476–486CrossRefGoogle Scholar
  54. Grote EE, Belnap J, Housman DC, Sparks JP (2010) Carbon exchange in biological soil crust communities under differential temperatures and soil water contents: implications for global change. Glob Change Biol 16:2763–2774CrossRefGoogle Scholar
  55. Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451:293–296PubMedCrossRefGoogle Scholar
  56. Haimovich-Dayan M, Kahlon S, Hihara Y, Hagemann M, Ogawa T, Ohad I, Lieman-Hurwitz J, Kaplan A (2011) Cross-talk between photomixotrophic growth and CO2-concentrating mechanism in Synechocystis sp. strain PCC 6803. Environ Microbiol 13:1767–1777PubMedCrossRefGoogle Scholar
  57. Hamerlynck EP, Tuba Z, Csintalan Z, Nagy Z, Henebry G, Goodin D (2000) Diurnal variation in photochemical dynamics and surface reflectance of the desiccation-tolerant moss, Tortula ruralis. Plant Ecol 151:55–63CrossRefGoogle Scholar
  58. Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293Google Scholar
  59. Horswill P, O’Sullivan O, Phoenix GK, Lee JA, Leake JR (2008) Base cation depletion, eutrophication and acidification of species-rich grasslands in response to long-term simulated nitrogen deposition. Environ Pollut 155:336–349PubMedCrossRefGoogle Scholar
  60. 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
  61. Hu R, Wang X, Pan Y, Zhang Y, Zhang H (2014) The response mechanisms of soil N mineralization under biological soil crusts to temperature and moisture in temperate desert regions. Eur J Soil Biol 62:66–73CrossRefGoogle Scholar
  62. Huxman TE, Hamerlynck EP, Moore BD, Smith SD, Jordan DN, Zitzer SF, Nowak RS, Coleman JS, Seemann JR (1998) Photosynthetic down-regulation in Larrea tridentata exposed to elevated atmospheric CO2: interaction with drought under glasshouse and field (FACE) exposure. Plant Cell Environ 21:1153–1161CrossRefGoogle Scholar
  63. IPCC (2013) Intergovernmental Panel on Climate Change 5th Assessment ReportGoogle Scholar
  64. Jauhiainen J, Silvola J (1999) Photosynthesis of Sphagnum fuscum at long-term raised CO2 concentrations. Annales Botanici Fennici 36:11–19Google Scholar
  65. Johnson SL, Kuske CR, Carney TD, Housman DC, Gallegos-Graves LV, Belnap J (2012) Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem. Glob Change Biol 18(8):2583–2593. doi: 10.1111/j.1365-2486.2012.02709.x
  66. Kimball B (2011) Comment on the comment by Amthor et al. on “Appropriate experimental ecosystem warming methods” by Aronson and McNulty. Agric For Meteorol 151:420–424CrossRefGoogle Scholar
  67. Ladron de Guevara M, Lázaro R, Quero JL, Ochoa V, Gozalo B, Berdugo M, Ucles O, Escolar C, Maestre FT (2014) Simulated climate change reduced the capacity of lichen-dominated biocrusts to act as carbon sinks in two semi-arid Mediterranean ecosystems. Biodivers Conserv 23:1787–1807CrossRefGoogle Scholar
  68. Lane RW, Menona M, McQuaida JB, Adams DG, Thomas AD, Hoon SR, Dougill AJ (2013) Laboratory analysis of the effects of elevated atmospheric carbon dioxide on respiration in biological soil crusts. J Arid Environ 98:52–59CrossRefGoogle Scholar
  69. Lang SI, Cornelissen JHC, Shaver GR, Ahrens M, Callaghan TV, Molau U, Ter Braak CJF, Hölzer A, Aerts R (2012) Arctic warming on two continents has consistent negative effects on lichen diversity and mixed effects on bryophyte diversity. Glob Change Biol 18:1096–1107CrossRefGoogle Scholar
  70. Lange OL (2002) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long-term field monitoring of CO2 exchange and its physiological interpretation. I. Dependence of photosynthesis on water content, light, temperature, and CO2 concentration from laboratory measurements. Flora 197:233–249CrossRefGoogle Scholar
  71. Lange OL, Green TGA (2005) Lichens show that fungi can acclimate their respiration to seasonal changes in temperature. Oecologia 142:11–19PubMedCrossRefGoogle Scholar
  72. Lange OL, Green TGA (2008) Diel and seasonal courses of ambient carbon dioxide concentration and their effect on productivity of the epilithic lichen Lecanora muralis in a temperate suburban habitat. Lichenologist 40:449–462CrossRefGoogle Scholar
  73. Lange OL, Green TGA, Reichenberger H (1999) The response of lichen photosynthesis to external CO2 concentration and its interaction with thallus water-status. J Plant Physiol 154:157–166CrossRefGoogle Scholar
  74. LeJeune K, Seastedt T (2001) Centaurea species: the forb that won the west. Conserv Biol 15:1568–1574CrossRefGoogle Scholar
  75. Lenhart K, Weber B, Elbert W, Steinkamp J, Clough T, Crutzen P, Pöschl U, Keppler F (2015) Nitrous oxide and methane emissions from cryptogamic covers. Glob Change Biol 21:3889–3900CrossRefGoogle Scholar
  76. Li SX, Wang ZH, Hu TT, Gao YJ, Stewart BA (2009) Nitrogen in dryland soils of China and its management. Adv Agron 101:123–181CrossRefGoogle Scholar
  77. Livina VN, Kwasniok F, Lohmann G, Kantelhardt JW, Lenton TM (2011) Changing climate states and stability: from Pliocene to present. Clim Dyn 37:2437–2453CrossRefGoogle Scholar
  78. Maestre FT, Escolar C, Martínez I, Escudero A (2008) Are soil lichen communities structured by biotic interactions? A null model analysis. J Veg Sci 19:261–266CrossRefGoogle Scholar
  79. Maestre FT, Martinez I, Escolar C, Escudero A (2009) On the relationship between abiotic stress and co-occurrence patterns: an assessment at the community level using soil lichen communities and multiple stress gradients. Oikos 118:1015–1022CrossRefGoogle Scholar
  80. Maestre FT, Bowker MA, Escolar C, Puche MD, Soliveres S, Maltez-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 Mediterranean plant and biological soil crust communities. Philos Trans R Soc B Biol Sci 365:2057–2070CrossRefGoogle Scholar
  81. Maestre FT, Salguero-Gómez R, Quero JL (2012) It’s getting hotter in here: determining and projecting the impacts of global change on drylands. Philos Trans R Soc B Biol Sci 3062–3075Google Scholar
  82. Maestre FT, Escolar C, Ladrón de Guevara M, Quero JL, Lázaro R, Delgado-Baquerizo M, Ochoa V, Berdugo M, Gozalo B, Gallardo A (2013) Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Glob Change Biol 19:3835–3847CrossRefGoogle Scholar
  83. Maphangwa KW, Musil CF, Raitt L, Zedda L (2012) Experimental climate warming decreases photosynthetic efficiency of lichens in an arid South African ecosystem. Oecologia 169:257–268PubMedCrossRefGoogle Scholar
  84. Marschall M, Proctor MC (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Ann Bot 94:593–603PubMedPubMedCentralCrossRefGoogle Scholar
  85. McCalley CK, Sparks JP (2009) Abiotic gas formation drives nitrogen loss from a desert ecosystem. Science 326:837–840PubMedCrossRefGoogle Scholar
  86. McHugh TA, Morrissey EM, Reed SC, Hungate BA, Schwartz E (2015) Water from air: an overlooked source of moisture in arid and semiarid regions. Sci Rep 5:13767PubMedPubMedCentralCrossRefGoogle Scholar
  87. Miralles I, Domingo F, García-Campos E, Trasar-Cepeda C, Leirós MC, Gil-Sotres F (2012) Biological and microbial activity in biological soil crusts from the Tabernas desert, a sub-arid zone in SE Spain. Soil Biol Biochem 55:113–121CrossRefGoogle Scholar
  88. Miralles I, Trasar-Cepeda C, Leiros MC, Gil-Sotres F (2013) Labile carbon in biological soil crusts in the Tabernas desert, SE Spain. Soil Biol Biochem 58:1–8CrossRefGoogle Scholar
  89. Miranda JD, Padilla FM, Pugnaire FI (2009) Response of a Mediterranean semiarid community to changing patterns of water supply. Perspect Plant Ecol Evol Syst 11:255–266CrossRefGoogle Scholar
  90. Mishler BD, Oliver MJ (2009) Putting Physcomitrella patens on the tree of life: the evolution and ecology of mosses. Annu Plant Rev 36:1–15Google Scholar
  91. Morgan JA, LeCain DR, Pendall E, Blumenthal DM, Kimball BA, Carrillo Y, Williams DG, Heisler-White J, Dijkstra FA, West M (2011) C4 grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland. Nature 476:202–205PubMedCrossRefGoogle Scholar
  92. Munson SM, Belnap J, Schelz CD, Moran M, Carolin TW (2011) On the brink of change: plant responses to climate on the Colorado Plateau. Ecosphere 2:Art 68CrossRefGoogle Scholar
  93. Neher DA, Weicht TR, Moorhead DL, Sinsabaugh RL (2004) Elevated CO2 alters functional attributes of nematode communities in forest soils. Funct Ecol 18:584–591CrossRefGoogle Scholar
  94. Neher DA, Lewins SA, Weicht TR, Darby BJ (2009) Microarthropod communities associated with biological soil crusts in the Colorado Plateau and Chihuahuan deserts. J Arid Environ 73:672–677CrossRefGoogle Scholar
  95. Norby RJ, Sigal LL (1989) Nitrogen fixation in the lichen Lobaria pulmonaria in elevated atmospheric carbon dioxide. Oecologia 79:566–568CrossRefGoogle Scholar
  96. Nowak RS, Zitzer SF, Babcock D, Smith-Longozo V, Charlet TN, Coleman JS, Seemann JR, Smith SD (2004) Elevated atmospheric CO2 does not conserve soil water in the Mojave Desert. Ecology 85:93–99CrossRefGoogle Scholar
  97. Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Evol Syst 4:25–51CrossRefGoogle Scholar
  98. Ochoa-Hueso R, Manrique E (2010) Nitrogen fertilization and water supply affect germination and plant establishment of the soil seed bank present in a semi-arid Mediterranean scrubland. Plant Ecol 210:263–273CrossRefGoogle Scholar
  99. Ochoa-Hueso R, Manrique E (2013) Effects of nitrogen deposition on growth and physiology of Pleurochaete squarrosa (Brid.) Lindb., a terricolous moss from Mediterranean ecosystems. Water Air Soil Pollut 224:1492CrossRefGoogle Scholar
  100. Ochoa-Hueso R, Manrique E (2014) Impacts of altered precipitation, nitrogen deposition and plant competition on a Mediterranean seedbank. J Veg Sci 25:1289–1298CrossRefGoogle Scholar
  101. Ochoa-Hueso R, Allen EB, Branquinho C, Cruz C, Dias T, Fenn ME, Manrique E, Pérez-Corona ME, Sheppard LJ, Stock WD (2011a) Nitrogen deposition effects on Mediterranean-type ecosystems: an ecological assessment. Environ Pollut 159:2265–2279PubMedCrossRefGoogle Scholar
  102. Ochoa-Hueso R, Hernandez RR, Pueyo JJ, Manrique E (2011b) Spatial distribution and physiology of biological soil crusts from semi-arid central Spain are related to soil chemistry and shrub cover. Soil Biol Biochem 43:1894–1901CrossRefGoogle Scholar
  103. Ochoa-Hueso R, Maestre FT, de los Ríos A, Valea S, Theobald MR, Vivanco MG, Manrique E, Bowker MA (2013a) Nitrogen deposition alters nitrogen cycling and reduces soil carbon content in low-productivity semiarid Mediterranean ecosystems. Environ Pollut 179:185–193PubMedPubMedCentralCrossRefGoogle Scholar
  104. Ochoa-Hueso R, Mejías-Sánz V, Pérez-Corona ME, Manrique E (2013b) Nitrogen deposition effects on tissue chemistry and phosphatase activity in Cladonia foliacea (Huds.) Willd., a common terricolous lichen of semiarid Mediterranean shrublands. J Arid Environ 88:78–81CrossRefGoogle Scholar
  105. Ochoa-Hueso R, Bell MD, Manrique E (2014) Impacts of increased nitrogen deposition and altered precipitation regimes on soil fertility and functioning in semiarid Mediterranean shrublands. J Arid Environ 104:106–115CrossRefGoogle Scholar
  106. Ojima DS, Dirks BOM, Glenn EP, Owensby CE, Scurlock JO (1993) Assessment of carbon budget for grasslands and drylands of the world. Water Air Soil Pollut 70:95–109CrossRefGoogle Scholar
  107. Oliver MJ, Velten J, Wood AJ (2000) Bryophytes as experimental models for the study of environmental stress tolerance: Tortula ruralis and desiccation tolerance in mosses. Plant Ecol 151:73–84CrossRefGoogle Scholar
  108. Oliver M, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats. Integr Comp Biol 45:788–799PubMedCrossRefGoogle Scholar
  109. Pardo LH, Fenn ME, Goodale CL, Geiser LH, Driscoll CT, Allen EB, Baron JS, Bobbink R, Bowman WD, Clark CM, Emmett B, Gilliam FS, Greaver TL, Hall SJ, Lilleskov EA, Liu L, Lynch JA, Nadelhoffer KJ, Perakis SS, Robin-Abbott MJ, Stoddard JL, Weathers KC, Dennis RL (2011) Effects of nitrogen deposition and empirical critical loads for nitrogen for ecological regions of the United States. Ecol Appl 21:3049–3082CrossRefGoogle Scholar
  110. Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2004) Stimulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol 161:279–289CrossRefGoogle Scholar
  111. Phoenix GK, Hicks WK, Cinderby S, Kuylenstierna JCI, Stock WD, Dentener FJ, Giller KE, Austin AT, Lefroy RDB, Gimeno BS, Ashmore MR, Ineson P (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Change Biol 12:470–476CrossRefGoogle Scholar
  112. Pinho P, Augusto S, Martins-Loução MA, Pereira MJ, Soares A, Máguas C, Branquinho C (2008) Causes for change in nitrophytic and oligotrophic lichens species in Mediterranean climate: impact of land-cover and atmospheric pollutants. Environ Pollut 154:380–389PubMedCrossRefGoogle Scholar
  113. Pinho P, Branquinho C, Cruz C, Tang YS, Dias T, Rosa AP, Máguas C, Martins-Loução MA, Sutton MA (2009) Assessment of critical levels of atmospheric ammonia for lichen diversity in cork-oak Woodland, Portugal. In: Reis S, Baker S (eds) Atmospheric ammonia. Detecting emission changes and environmental impacts. Results of an Expert Workshop under the Convention on long-range transboundary air pollution. Springer Science, Sutton, MA, pp 109–119Google Scholar
  114. Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562PubMedCrossRefGoogle Scholar
  115. Poorter H (1993) Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. Vegetatio 104–105:77–97CrossRefGoogle Scholar
  116. Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198CrossRefGoogle Scholar
  117. Porada P, Weber B, Elbert W, Pöschl U, Kleidon A (2013) Estimating global carbon uptake by lichens and bryophytes with a process-based model. Biogeosciences 10:6989–7033CrossRefGoogle Scholar
  118. Porada P, Weber B, Elbert W, Pöschl U, Kleidon A (2014) Estimating impacts of lichens and bryophytes on global biogeochemical cycles. Glob Biogeochem Cycles 28:71–85CrossRefGoogle Scholar
  119. Potts DL, Huxman TE, Enquist BJ, Weltzin JF, Williams DG (2006) Resilience and resistance of ecosystem functional responses to a precipitation pulse in a semi-arid grassland. J Ecol 94:23–30CrossRefGoogle Scholar
  120. Proctor MC, Smirnoff N (2000) Rapid recovery of photosystems on rewetting desiccation-tolerant mosses: chlorophyll fluorescence and inhibitor experiments. J Exp Bot 51:1695–1704PubMedCrossRefGoogle Scholar
  121. Proctor MC, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD (2007) Desiccation-tolerance in bryophytes: a review. Bryologist 110:595–621CrossRefGoogle Scholar
  122. Pumpanen J, Ilvesniemi H, Perämäki M, Hari P (2003) Seasonal patterns of soil CO2 efflux and soil air CO2 concentration in a Scots pine forest: comparison of two chamber techniques. Glob Change Biol 9:371–382CrossRefGoogle Scholar
  123. Rao LE, Parker DR, Bytnerowicz A, Allen EB (2010) Nitrogen mineralization across an atmospheric nitrogen deposition gradient in Southern California deserts. J Arid Environ 73:920–930CrossRefGoogle Scholar
  124. Reed SC, Seastedt TR, Mann CM, Suding KN, Townsend AR, Cherwin KL (2007) Phosphorus fertilization stimulates nitrogen fixation and increases inorganic nitrogen concentrations in a restored prairie. Appl Soil Ecol 36:238–242CrossRefGoogle Scholar
  125. Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512CrossRefGoogle Scholar
  126. Reed SC, Coe KK, Sparks JP, Housman DC, Zelikova TJ, Belnap J (2012) Changes to dryland rainfall result in rapid moss mortality and altered soil fertility. Nat Clim Change 2:752–755. doi: 10.1038/NCLIMATE1596
  127. Rey A (2015) Mind the gap: non-biological processes contributing to soil CO2 efflux. Glob Change Biol 21:1752–1761CrossRefGoogle Scholar
  128. Reynolds JF, Smith DMS, Lambin EF, Turner BL II, Mortimore M, Batterbury SPJ, Downing TE, Dowlatabadi H, Fernández 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
  129. Sala OE, Lauenroth WK (1982) Small rainfall events: an ecological role in semiarid regions. Oecologia 53:301–304CrossRefGoogle Scholar
  130. Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774PubMedCrossRefGoogle Scholar
  131. Sardans J, Rodà F, Peñuelas J (2006) Effects of a nutrient pulse supply on nutrient status on the Mediterranean trees Quercus ilex subsp. ballota and Pinus halepensis on different soils and under different competitive pressure. Trees 20:619–632CrossRefGoogle Scholar
  132. Schwinning S, Sala OE, Loik ME, Ehleringer JR (2004) Thresholds, memory, and seasonality: understanding pulse dynamics in arid/semi-arid ecosystems. Oecologia 141:191–193PubMedCrossRefGoogle Scholar
  133. Shaw MR, Zavaleta ES, Chiariello NR, Cleland EE, Mooney HA, Field CB (2002) Grassland responses to global environmental changes suppressed by elevated CO2. Science 298:1987–1990PubMedCrossRefGoogle Scholar
  134. Shen W, Reynolds JF, Hui D (2009) Responses of dryland soil respiration and soil carbon pool size to abrupt versus gradual and individual versus combined changes in soil temperature, precipitation, and atmospheric [CO2]: a simulation analysis. Glob Change Biol 15:2274–2294CrossRefGoogle Scholar
  135. Sheridan RP (1979) Effects of airborne particulates on nitrogen fixation in legumes and algae. Phytopathology 69:1011–1018CrossRefGoogle Scholar
  136. Smith SD, Huxman TE, Zitzer SF, Charlet TN, Housman DC, Coleman JS, Fenstermaker LK, Seemann JR, Nowak RS (2000) Elevated CO2 increases productivity and invasive species success in an arid ecosystem. Nature 408:79–82PubMedCrossRefGoogle Scholar
  137. Steven B, Gallegos-Graves LV, Yeager CM, Belnap J, Evans RD, Kuske CR (2012) Dryland biological soil crust cyanobacteria show unexpected decreases in abundance under long-term elevated CO2. Environ Microbiol 14(12):3247–3258. doi: 10.1111/1462-2920.12011
  138. Steven B, Kuske CR, Gallegos-Graves V, Reed SC, Belnap J (2015) Climate change and physical disturbance manipulations result in distinct biological soil crust communities. Appl Environ Microbiol 81:7448–7459PubMedPubMedCentralCrossRefGoogle Scholar
  139. Su Y, Zhao X, Li A, Li X, Huang G (2011) Nitrogen fixation in biological soil crusts from the Tengger desert, northern China. Eur J Soil Biol 47:182–187CrossRefGoogle Scholar
  140. Suding KN, LeJeune KD, Seastedt TR (2004) Competitive impacts and responses of an invasive weed: dependencies on nitrogen and phosphorus availability. Oecologia 141:526–535PubMedCrossRefGoogle Scholar
  141. Toet S, Cornelissen JHC, Aerts R, van Logtestijn RSP, de Beus M, Stoevelaar R (2006) Moss responses to elevated CO2 and variation in hydrology in a temperate lowland peatland. Plant Ecol 182:27–40CrossRefGoogle Scholar
  142. Tuba Z, Csintalan Z, Szente K, Nagy Z, Grace J (1998) Carbon gains by desiccation-tolerant plants at elevated CO2. Funct Ecol 12:39–44CrossRefGoogle Scholar
  143. Van den Berg LJL, Gomassen HBM, Roelofs JGM, Bobbink R (2005) Effects of nitrogen enrichment on a coastal dune grassland: a mesocosm study. Environ Pollut 138:77–85PubMedCrossRefGoogle Scholar
  144. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B Biol Sci 272:2561–2569CrossRefGoogle Scholar
  145. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  146. Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos Trans R Soc B Biol Sci 368:20130119CrossRefGoogle Scholar
  147. Wand SJE, Midgley GF, Jones MH, Curtis PS (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Glob Change Biol 5:723–741CrossRefGoogle Scholar
  148. Weber B, Wu D, Tamm A, Ruckteschler N, Rodríguez-Caballero E, Steinkamp J, Meusel H, Elbert W, Behrendt T, Sörgel M, Cheng Y, Crutzen PJ, Su H, Pöschl U (2015) Biological soil crusts accelerate the nitrogen cycle through large NO and HONO emissions in drylands. Proc Natl Acad Sci U S A 112:15384–15389PubMedPubMedCentralCrossRefGoogle Scholar
  149. Weier KL, Doran JW, Power JF, Walters DT (1993) Denitrification and the dinitrogen nitrous-oxide ratio as affected by soil water, available carbon, and nitrate. Soil Sci Soc Am J 57:66–72CrossRefGoogle Scholar
  150. Weltzin JF, Loik ME, Schwinning S, Williams DG, Fay PA, Haddad BM, Harte J, Huxman TE, Knapp AK, Lin G, Pockman WT, Shaw MR, Small EE, Smith MD, Smith SD, Tissue DT, Zak JC (2003) Assessing the response of terrestrial ecosystems to potential changes in precipitation. BioScience 53:941–952CrossRefGoogle Scholar
  151. Wertin TM, Phillips SL, Reed SC, Belnap J (2012) Elevated CO2 did not mitigate the effect of a short-term drought on biological soil crusts. Biol Fertil Soils 48:797–805CrossRefGoogle Scholar
  152. Wertin TM, Reed SC, Belnap J (2015) C3 and C4 plant responses to increased temperatures and altered monsoonal precipitation in a cool desert on the Colorado Plateau, USA. Oecologia 177:997–1013PubMedCrossRefGoogle Scholar
  153. Yeager CM, Kornosky JL, Housman DC, Grote EE, Belnap J, Kuske CR (2004) Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Appl Environ Microbiol 70:973–983PubMedPubMedCentralCrossRefGoogle Scholar
  154. Yeager CM, Kuske CR, Carney TD, Johnson SL, Ticknor LO, Belnap J (2012) Response of biological soil crust diazotrophs to season, altered summer precipitation, and year-round increased temperature in an arid grassland of the Colorado Plateau, USA. Front Microbiol 3:1–14CrossRefGoogle Scholar
  155. Zelikova TJ, Housman DC, Grote EE, Neher DA, Belnap J (2012) Warming and increased precipitation frequency on the Colorado Plateau: implications for biological soil crusts and soil processes. Plant Soil 355:265–282CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland (outside the USA) 2016

Authors and Affiliations

  • Sasha C. Reed
    • 1
  • Fernando T. Maestre
    • 2
  • Raúl Ochoa-Hueso
    • 3
  • Cheryl R. Kuske
    • 4
  • Anthony Darrouzet-Nardi
    • 5
  • Mel Oliver
    • 6
  • Brian Darby
    • 7
  • Leopoldo G. Sancho
    • 8
  • Robert L. Sinsabaugh
    • 9
  • Jayne Belnap
    • 1
  1. 1.Southwest Biological Science CenterU.S. Geological SurveyMoabUSA
  2. 2.Area de Biodiversidad y Conservacion, Departamento de Biología y Geología, Física y Química Inorgánica, ESCETUniversidad Rey Juan CarlosMóstolesSpain
  3. 3.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityPenrithAustralia
  4. 4.Bioscience DivisionLos Alamos National LaboratoryLos AlamosUSA
  5. 5.Biological Sciences DepartmentUniversity of Texas at El PasoEl PasoUSA
  6. 6.USDA-ARS, Plant Genetics Research UnitUniversity of MissouriColumbiaUSA
  7. 7.Department of BiologyUniversity of North DakotaGrand ForksUSA
  8. 8.Departamento de Biologia Vegetal II, Facultad de FarmaciaUniversidad ComplutenseMadridSpain
  9. 9.Department of BiologyUniversity of New MexicoAlbuquerqueUSA

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