Carbon Budgets of Biological Soil Crusts at Micro-, Meso-, and Global Scales

  • Leopoldo G. SanchoEmail author
  • Jayne Belnap
  • Claudia Colesie
  • Jose Raggio
  • Bettina Weber
Part of the Ecological Studies book series (ECOLSTUD, volume 226)


The importance of biocrusts in the ecology of arid lands across all continents is widely recognized. In spite of this broad distribution, contributions of biocrusts to the global biogeochemical cycles have only recently been considered. While these studies opened a new view on the global role of biocrusts, they also clearly revealed the lack of data for many habitats and of overall standards for measurements and analysis. In order to understand carbon cycling in biocrusts and the progress which has been made during the last 15 years, we offer a multiscale approach covering different climatic regions. We also include a discussion on available measurement techniques at each scale: A microscale section focuses on the individual organism level, including modeling based on the combination of field and lab data. The mesoscale section addresses the CO2 exchange of a complete ecosystem or at the community level. Finally, we consider the contribution of biocrusts at a global scale, giving a general perspective of the most relevant findings regarding the role of biological soil crusts in the global terrestrial carbon cycle.


Gross Primary Production Dark Respiration Biological Soil Crust Total Soil Respiration Snow Free Season 
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.



L.G. Sancho and J. Raggio were supported by the Ministerio de Economía y Competitividad of Spain (projects CTM2012-38222-C01 and SCIN). Bettina Weber was supported by the Max Planck Society (Nobel Laureate Fellowship) and the German Research Foundation (project WE2393/2). We are especially thankful to Prof. T.G. Allan Green (Universidad Complutense Madrid) for advice and support. JB was supported by USGS Ecosystems program. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.


  1. Armstrong RA, Bradwell T (2010) Growth of crustose lichens: a review. Geogr Ann A 92:3–17CrossRefGoogle Scholar
  2. Bader MY, Zotz G, Lange OL (2010) How to minimize the sampling effort for obtaining reliable estimates of diel and annual CO2 budgets in lichens. Lichenologist 42:97–111CrossRefGoogle Scholar
  3. Belnap J (2002) Nitrogen fixation in biological soil crust from southeast Utah, USA. Biol Fertil Soils 35:128–135CrossRefGoogle Scholar
  4. Belnap J, Lange OL (eds) (2003) Biological soil crusts: structure, function and management, vol 150, 2nd edn, Ecological Studies. Springer, New YorkGoogle Scholar
  5. Billings WD (1987) Carbon balance of Alaskan tundra and taiga ecosystems: past, present and future. Quat Sci Rev 6:165–177CrossRefGoogle Scholar
  6. Bisbee KE, Gower ST, Norman JM, Nordheim EV (2001) Environmental controls on ground cover species composition and productivity in a boreal black spruce forest. Oecologia 129:261–270CrossRefGoogle Scholar
  7. Bowling DR, Bethers-Marchetti S, Lunch CK, Grote EE, Belnap J (2010) Carbon, water, and energy fluxes in a semiarid cold desert grassland during and following multiyear drought. J Geophys Res 115:G04026. doi: 10.1029/2010JG001322 CrossRefGoogle Scholar
  8. Bowling DR, Grote EE, Belnap J (2011) Rain pulse response of soil CO2 exchange by biological soil crusts and grasslands of the semiarid Colorado Plateau, United States. J Geophys Res 116:G04006. doi: 10.1029/2011JG001722 Google Scholar
  9. Brostoff WN, Sharifi MR, Rundel PW (2005) Photosynthesis of cryptobiotic soil crusts in a seasonally inundated system of pans and dunes in the western Mojave Desert, CA: field studies. Flora 200:592–600CrossRefGoogle Scholar
  10. Büdel B, Colesie C, Green TGA, Grube M, Lazaro-Suau R, Loewen-Schneider K, Maier S, Peer T, Pintado A, Raggio J, Ruprecht U, Sancho L, Schroeter B, Türk R, Weber B, Wedin M, Westberg M, Williams L, Zheng L (2014) Improved appreciation of the functioning and importance of biological soil crusts in Europe—the Soil Crust International project (SCIN). Biodivers Conserv 23:1639–1658CrossRefPubMedPubMedCentralGoogle Scholar
  11. Castillo-Monroy AP, Maestre FT, Rey A, Soliveres S, García-Palacios P (2011) Biological soil crust microsites are the main contributor to soil respiration in semiarid ecosystem. Ecosystems 18:835–847CrossRefGoogle Scholar
  12. Chapin FS III, Woodwell GM, Randerson JT et al (2006) Reconciling carbon-cycling concepts, terminology and methods. Ecosystems 9:1041–1050CrossRefGoogle Scholar
  13. Colesie C, Green TGA, Haferkamp I, Büdel B (2014) Habitat stress initiates changes in composition, CO2 gas exchange and C-allocation as life traits in biological soil crusts. ISME J 8:2104–2115CrossRefPubMedPubMedCentralGoogle Scholar
  14. Coxson DS, Marsh J (2001) Lichen chronosequences (postfire and postharvest) in lodgepole pine (Pinus contorta) forests of northern interior British Columbia. Can J Bot 79:1449–1464Google Scholar
  15. 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(3):363–378CrossRefGoogle Scholar
  16. 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
  17. Evans RD, Lange OL (2003) Biological soil crusts and ecosystem nitrogen and carbon dynamics. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function and management, vol 150, 2nd edn, Ecological Studies. Springer, HeidelbergGoogle Scholar
  18. Feng W, Zhang Y, Wu B, Qin S, Lai Z (2014) Influence of environmental factors on carbon dioxide exchange in biological soil crusts in desert areas. Arid Land Res Manag 28:186–196CrossRefGoogle Scholar
  19. Fenton JHC (1980) The rate of peat accumulation in Antarctic moss banks. J Ecol 68:211–228CrossRefGoogle Scholar
  20. García-Pichel F, Belnap J (1996) Microenvironments and microscale productivity of cyanobacteria desert crusts. J Phycol 32:774–782CrossRefGoogle Scholar
  21. Green TGA, Lange OL, Cowan IR (1994) Ecophysiology of lichen photosynthesis: the role of water status and thallus diffusion resistances. Cryptogam Bot 4:166–178Google Scholar
  22. 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 Chang Biol 16:2763–2774CrossRefGoogle Scholar
  23. 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
  24. Innes JL (1988) The use of lichens in dating. In: Galun M (ed) Handbook of lichenology, vol III. CRC Press, Boca Raton, pp 75–92Google Scholar
  25. Jeffries DL, Link SO, Klopatek JM (1993) CO2 fluxes of a cryptogamic crust. Response to resaturation. New Phytol 125:163–173CrossRefGoogle Scholar
  26. Klopatek JM (1992) Cryptogamic crusts as potential indicators of disturbance in semi-arid landscapes. In: McKenzie DE, Wyatt E, McDonald VJ (eds) Ecological indicators. Elsevier, New York, pp 773–786CrossRefGoogle Scholar
  27. Lange OL (2000) Photosynthetic performance of gelatinous lichen under temperate habitat conditions: long-term monitoring of CO2 exchange of Collema cristatum. Bibl Lichenol 75:307–332Google Scholar
  28. Lange OL (2002) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long-term field monitoring of CO2 exchange and its physiological interpretation: dependence of photosynthesis on water content, light, temperature, and CO2 concentration from laboratory measurements. Flora 197:233–249CrossRefGoogle Scholar
  29. Lange OL (2003a) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long-term field monitoring of CO2 exchange and its physiological interpretation: III Diel, seasonal and annual carbon budgets. Flora 198:277–292Google Scholar
  30. Lange OL (2003b) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long term field monitoring of CO2 exchange and its physiological interpretation. II. Diel and seasonal patterns of net photosynthesis and respiration. Flora 198:55–70Google Scholar
  31. Lange OL, Green TGA (2004) Photosynthetic performance of the squamulose-soil crust lichen Squamarina lentigera: laboratory measurements and long term monitoring of CO2 exchange in the field. Bibl Lichenol 88:363–390Google Scholar
  32. Lange OL, Kidron GJ, Büdel B, Meyer A, Kilian E, Abeliovich A (1992) Taxonomic composition and the photosynthetic characteristics of the “biological soilcrusts” covering sand dunes in the western Negev Desert. Funct Ecol 6:519–527CrossRefGoogle Scholar
  33. Lange OL, Meyer A, Zellner H, Heber U (1994) Photosynthesis and water relations of lichen soil crusts: field measurements in the coastal fog zone of the Namib Desert. Funct Ecol 8:253–264CrossRefGoogle Scholar
  34. Lange OL, Reichenberger H, Meyer A (1995) High thallus water content and photosynthetic CO2 exchange of lichens. Laboratory experiments with soil crust species from local xerothermic steppe formations in Franconia, Germany. In: Daniels F, Schulz M, Peine J (eds) Flechten Follmann: contributions to lichenology in honour of Gerhard Follmann. Geobotanical and Phytotaxonomical Study Group, Universitat Koln, Cologne, pp 139–153Google Scholar
  35. Lange OL, Belnap J, Reichenberger H, Meyer A (1997a) Photosynthesis of green algal soil crust lichens from arid lands in southern Utah, USA: role of water content on light and temperature responses of CO2 exchange. Flora 192:1–15Google Scholar
  36. Lange OL, Reichenberger H, Walz H (1997b) Continuous monitoring of CO2 exchange of lichens in the field: short-term enclosure with an automatically operating cuvette. Lichenologist 29:259–274Google Scholar
  37. Lange OL, Hahn S, Meyer A, Tenhunen JD (1998) Upland tundra in the foothills of the Brooks Range, Alaska, USA: lichen long-term photosynthetic CO2 uptake and net carbon gain. Arct Alp Res 3:232–261Google Scholar
  38. Lange OL, Green TGA, Melzer B, Meyer A, Zellner H (2006) Water relations and CO2 exchange of the terrestrial lichen Teloschistes capensis in the Namib fog Desert: measurements during two seasons in the field and under controlled conditions. Flora 16:268–280CrossRefGoogle Scholar
  39. Ma J, Wang ZY, Stevenson BA, Zheng XJ, Li Y (2013) An inorganic CO2 diffusion and dissolution process explain negative CO2 fluxes in saline/alkaline soils. Sci Rep 3:2025PubMedPubMedCentralGoogle Scholar
  40. 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 stress gradients? Insights from semi-arid plant and biological soil crust communities. Philos Trans R Soc Lond B Biol Sci 365:2057–2070CrossRefPubMedPubMedCentralGoogle Scholar
  41. Maestre FT, Escolar C, Ladrón De Guevara M, Quero JL, Lázaro R, Delgado-Baquerizo M, Ochoa M, Berdugo M, Gozalo B, Gallardo A (2013) Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Glob Chang Biol 19:3835–3847CrossRefPubMedPubMedCentralGoogle Scholar
  42. Murray KJ, Harley PC, Beyers J, Walz H, Tenhunen JD (1989) Water content effects on photosynthetic response of Sphagnum mosses from the foothills of the Philip Smith Mountains, Alaska. Oecologia 79:224–250CrossRefGoogle Scholar
  43. Oechel WC, Collins NJ (1976) Comparative CO2 exchange patterns in mosses from two tundra habitats at Barrow, Alaska. Can J Bot 54:1355–1369CrossRefGoogle Scholar
  44. Pintado A, Sancho LG, Blanquer JM, Green TGA, Lázaro R (2010) Microclimatic factors and photosynthetic activity of crustose lichens from the semiarid southeast of Spain: long-term measurements for Diploschistes diacapsis. Bibl Lichenol 105:211–224Google Scholar
  45. 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
  46. Porada P, Weber B, Elbert W, Pöschl U, Kleidon A (2014) Estimating impacts of lichens and bryophytes on global biogeochemical cycles. Global biogeochemical cycles early view. Glob Biogeochem Cycles 28:71–85CrossRefGoogle Scholar
  47. Raggio J, Green TGA, Crittenden PD, Pintado A, Vivas M, Pérez-Ortega S, De los Ríos A, Sancho LG (2012) Comparative ecophysiology of three Placopsis species, pioneer lichens in recently exposed Chilean glacial forelands. Symbiosis 56:55–66CrossRefGoogle Scholar
  48. Raggio J, Pintado A, Vivas M, Sancho LG, Büdel B, Colesie C, Weber B, Schroeter B, Green TGA (2014) Continuous chlorophyll fluorescence, gas exchange and microclimate monitoring in a natural soil crust habitat in Tabernas badlands, Almeria, Spain: progressing towards a model to understand productivity. Biodivers Conserv 23:1809–1826CrossRefGoogle Scholar
  49. Randerson JT, Chapin FSIII, Harden JW, Neef JC, Harmon ME (2002) Net ecosystem production: a comprehensive measure of net carbon accumulation by ecosystems. Ecol Appl 12:937–947CrossRefGoogle Scholar
  50. Rey A (2015) Mind the gap: non-biological processes contributing to soil CO2 efflux. Glob Chang Biol 21:1752–1761CrossRefPubMedGoogle Scholar
  51. Rey A, Belelli-Marchesini L, Etiope G, Papale D, Canfora E, Valentini R, Pegoraro E (2014) Partitioning the net ecosystem carbon balance of a semiarid steppe into biological and geological components. Biogeochemistry 118:83–101CrossRefGoogle Scholar
  52. Roberts SJ, Hodgson DA, Shelley S, Royles J, Griffiths HS, Deen TJ, Thorne MAS (2010) Establishing lichenometric ages for nineteenth- and twentieth-century glacier fluctuations on South Georgia (South Atlantic). Geogr Ann A 92:125–139CrossRefGoogle Scholar
  53. Sancho L, Pintado A (2004) Evidence of high annual growth rate for lichens in the maritime Antarctic. Polar Biol 27:312–319CrossRefGoogle Scholar
  54. Sancho LG, Palacios D, Green TGA, Vivas M, Pintado A (2011) Extreme high lichens growth rates detected in recently deglaciated areas in Tierra del Fuego. Polar Biol 34:813–822CrossRefGoogle Scholar
  55. Schlensog M, Schroeter B (2001) A new method for the accurate in situ monitoring of chlorophyll a fluorescence in lichen and bryophytes. Lichenologist 33:443–452CrossRefGoogle Scholar
  56. Schroeter B, Green TGA, Seppekt RD, Kappen L (1992) Monitoring photosynthetic activity of crustose lichens using a PAM-2000 fluorescence system. Oecologia 92:457–465CrossRefGoogle Scholar
  57. Schuur EAG, Crummer KG, Vogel JG, Mack MC (2007) Plant species composition and productivity following permafrost thaw and thermokarst in Alaskan tundra. Ecosytems 10:280–292CrossRefGoogle Scholar
  58. Serna-Perez A, Monger HC, Herrick JE, Murray L (2006) Carbon dioxide emissions from exhumed petrocalcic horizons. Soil Sci Soc Am J 70:795–805CrossRefGoogle Scholar
  59. Shanhun FL, Almond PC, Clough TJ, Smith CMS (2012) Abiotic processes dominate CO2 fluxes in Antarctic soils. Soil Biol Biochem 53:99–111CrossRefGoogle Scholar
  60. Shaver GR, Chapin FS (1991) Production: biomass relationships and element cycling in contrasting arctic vegetation types. Ecol Monogr 61:1–31CrossRefGoogle Scholar
  61. Sommerkorn M, Bölter M, Kappen L (1999) Carbon dioxide fluxes of soils and mosses in wet tundra of Taimyr Peninsula, Siberia: controlling factors and contribution to net system fluxes. Polar Res 18:253–260CrossRefGoogle Scholar
  62. Sponseller RA (2007) Precipitation pulses and soil CO2 efflux in a Sonoran Desert ecosystem. Glob Chang Biol 13:426–436CrossRefGoogle Scholar
  63. Su YG, Wu L, Zhang YM (2012) Characteristics of carbon flux in two biologically crusted soils in the Gurbantunggut Desert, Northwestern China. Catena 96:41–48CrossRefGoogle Scholar
  64. Su YG, Wu L, Zhou ZB, Zhang YM (2013) Carbon flux in deserts depends on soil cover type: a case study in the Gurbantunggut Desert, North China. Soil Biol Biochem 58:332–340CrossRefGoogle Scholar
  65. Tenhunen JD, Lange OL, Hahn S, Siegwolf R, Oberbauer SF (1992) The ecosystem role of poikilohydric tundra plants. In: Chapin FS, Jefferies RL, Reynolds JF, Shaver GR, Svoboda J (eds) Arctic ecosystems in a changing climate. Academic Press, San DiegoGoogle Scholar
  66. Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryologist 106:395–409CrossRefGoogle Scholar
  67. Uchida M, Muraoka H, Nakatsubo T, Bekku Y, Ueno T, Kanda H, Koizumi H (2002) Net photosynthesis, respiration and production of the moss Sanionia uncinata on a glacier foreland in the high arctic, Ny-Alesund, Svalbard. Arct Antarct Alp Res 34:287–292CrossRefGoogle Scholar
  68. Uchida M, Nakatsubo T, Kanda H, Koizumi H (2006) Estimation of the annual primary production of the lichen Cetrariella delisei in a glacier foreland on the high arctic, Ny-Alesund, Svalbard. Polar Res 25:39–49CrossRefGoogle Scholar
  69. Weber B, Graf T, Bass M (2012) Ecophysiological analyses of moss-dominated biological soil-crusts and their separate components from the Succulent Karoo, South Africa. Planta 236:129–139CrossRefPubMedGoogle Scholar
  70. Weber B, Berkemeier T, Ruckteschler N, Caesar J, Heintz H, Ritter H, Braß H (2016) Development and calibration of a novel sensor to analyze the water content of biological soil crusts and surface soils. Methods Ecol Evol. 7(1):14–22. doi: 10.1111/2041-210X.12459 Google Scholar
  71. Wilske B, Burgheimer J, Maseyk K, Karnieli A, Zaady E, Andreae MO, Yakir D, Kesselmeier J (2009) Modelling the variability in annual carbon fluxes related to biological soil crusts in a Mediterranean shrubland. Biogeosci Discuss 6:7295–7324CrossRefGoogle Scholar
  72. Winchester V, Harrison S (2000) Dendrochronology and lichenometry: colonization, growth rates and dating of geomorphological events on the east side of the North Patagonian Icefield, Chile. Geomorphology 34:181–194CrossRefGoogle Scholar
  73. Xie J, Li Y, Zhai C, Li C, Lan Z (2009) CO2 absorption by alkaline soils an its implication to the global carbon cycle. Environ Geol 56:953–961CrossRefGoogle Scholar
  74. Zaady E, Kuhn U, Wilske B, Sandoval-Soto L, Kesselmeier J (2000) Patterns of CO2 exchange in biological soil crusts of successional stages. Soil Biol Biochem 32:959–966CrossRefGoogle Scholar
  75. Zhao MS, Heinsch FA, Nemani RR et al (2005) Improvements of the MODIS terrestrial gross and net primary production global data set. Remote Sens Environ 95:164–176CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Leopoldo G. Sancho
    • 1
    Email author
  • Jayne Belnap
    • 2
  • Claudia Colesie
    • 3
  • Jose Raggio
    • 1
  • Bettina Weber
    • 4
  1. 1.Facultad de Farmacia, Departamento de Biologıa Vegetal IIUniversidad ComplutenseMadridSpain
  2. 2.US Geological Survey, Southwest Biological Science CenterCanyonlands Research StationMoabUSA
  3. 3.Faculty of Biology, Plant Ecology and SystematicsUniversity of KaiserslauternKaiserslauternGermany
  4. 4.Multiphase Chemistry DepartmentMax Planck Institute for ChemistryMainzGermany

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