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Ecosystems

, Volume 22, Issue 1, pp 15–32 | Cite as

Climatic Sensitivity of Dryland Soil CO2 Fluxes Differs Dramatically with Biological Soil Crust Successional State

  • Colin L. TuckerEmail author
  • Scott Ferrenberg
  • Sasha C. Reed
Article

Abstract

Arid and semiarid ecosystems make up approximately 41% of Earth’s terrestrial surface and are suggested to regulate the trend and interannual variability of the global terrestrial carbon (C) sink. Biological soil crusts (biocrusts) are common dryland soil surface communities of bryophytes, lichens, and/or cyanobacteria that bind the soil surface together and that may play an important role in regulating the climatic sensitivity of the dryland C cycle. Major uncertainties exist in our understanding of the interacting effects of changing temperature and moisture on CO2 uptake (photosynthesis) and loss (respiration) from biocrust and sub-crust soil, particularly as related to biocrust successional state. Here, we used a mesocosm approach to assess how biocrust successional states related to climate treatments. We subjected bare soil (Bare), early successional lightly pigmented cyanobacterial biocrust (Early), and late successional darkly pigmented moss-lichen biocrust (Late) to either ambient or + 5°C above ambient soil temperature for 84 days. Under ambient temperatures, Late biocrust mesocosms showed frequent net uptake of CO2, whereas Bare soil, Early biocrust, and warmed Late biocrust mesocosms mostly lost CO2 to the atmosphere. The inhibiting effect of warming on CO2 exchange was a result of accelerated drying of biocrust and soil. We used these data to parameterize, via Bayesian methods, a model of ecosystem CO2 fluxes, and evaluated the model with data from an autochamber CO2 system at our field site on the Colorado Plateau in SE Utah. In the context of the field experiment, the data underscore the negative effect of warming on fluxes both biocrust CO2 uptake and loss—which, because biocrusts are a dominant land cover type in this ecosystem, may extend to ecosystem-scale C cycling.

Keywords

Bayesian statistics biological soil crust ecosystem model gross primary production moisture sensitivity net soil exchange semiarid shrublands soil respiration temperature sensitivity 

Notes

Acknowledgements

This material is based upon work supported by US Department of Energy Office of Science, Office of Biological and Environmental Research Terrestrial Ecosystem Sciences Program, under Award Number DE-SC-0008168 and by US Geological Survey Ecosystems Mission Area. We appreciate everyone who worked on this project, especially Armin Howell, Robin Reibold, Rose Egelhoff and Paige Austin. We thank Anthony Darrouzet-Nardi for valuable feedback on the manuscript. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.

Supplementary material

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References

  1. Ahlström A, Raupach MR, Schurgers G, Smith B, Arneth A, Jung M, Reichstein M, Canadell JG, Friedlingstein P, Jain AK, Kato E, Poulter B, Sitch S, Stocker BD, Viovy N, Wang YP, Wiltshire A, Zaehle S, Zeng N. 2015. The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science 348:895–9.CrossRefGoogle Scholar
  2. Atkin OK, Tjoelker MG. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in plant science 8:343–51.CrossRefGoogle Scholar
  3. Austin A, Yahdjian L, Stark J, Belnap J, Porporato A, Norton U, Ravetta D, Schaeffer S. 2004. Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–35.CrossRefGoogle Scholar
  4. Barger NN, Weber B, Garcia-Pichel F, Zaady E, Belnap J. 2016. Patterns and controls on nitrogen cycling of biological soil crusts. Biological soil crusts: an organizing principle in drylands. Berlin: Springer. pp 257–85.CrossRefGoogle Scholar
  5. Belnap J. 1995. Surface disturbances: their role in accelerating desertification. Desertification in developed countries. Berlin: Springer. pp 39–57.CrossRefGoogle Scholar
  6. Belnap J. 2002. Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fertil Soils 35:128–35.CrossRefGoogle Scholar
  7. Belnap J, Phillips SL, Miller ME. 2004. Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia 141:306–16.CrossRefGoogle Scholar
  8. Belnap J, Weber B, Büdel B. 2016. Biological soil crusts as an organizing principle in drylands. Biological soil crusts: an organizing principle in drylands. Berlin: Springer. pp 3–13.CrossRefGoogle Scholar
  9. Bowker MA, Belnap J, Büdel B, Sannier C, Pietrasiak N, Eldridge DJ, Rivera-Aguilar V. 2016. Controls on distribution patterns of biological soil crusts at micro-to global scales. Biological soil crusts: an organizing principle in drylands. Berlin: Springer. pp 173–97.CrossRefGoogle Scholar
  10. Bowker MA, Maestre FT, Eldridge D, Belnap J, Castillo-Monroy A, Escolar C, Soliveres S. 2014. Biological soil crusts (biocrusts) as a model system in community, landscape and ecosystem ecology. Biodivers Conserv 23:1619–37.CrossRefGoogle Scholar
  11. Bowker MA, Mau RL, Maestre FT, Escolar C, Castillo-Monroy AP. 2011. Functional profiles reveal unique ecological roles of various biological soil crust organisms. Funct Ecol 25:787–95.CrossRefGoogle Scholar
  12. Burgheimer J, Wilske B, Maseyk K, Karnieli A, Zaady E, Yakir D, Kesselmeier J. 2006. Relationships between normalized difference vegetation index (NDVI) and carbon fluxes of biologic soil crusts assessed by ground measurements. J Arid Environ 64:651–69.CrossRefGoogle Scholar
  13. Castillo-Monroy AP, Bowker MA, Maestre FT, Rodriguez-Echeverria S, Martinez I, Barraza-Zepeda CE, Escolar C. 2011a. Relationships between biological soil crusts, bacterial diversity and abundance, and ecosystem functioning: Insights from a semi-arid Mediterranean environment. J Veg Sci 22:165–74.CrossRefGoogle Scholar
  14. Castillo-Monroy AP, Maestre FT, Rey A, Soliveres S, Garcia-Palacios P. 2011b. Biological soil crust microsites are the main contributor to soil respiration in a semiarid ecosystem. Ecosystems 14:835–47.CrossRefGoogle Scholar
  15. Coe KK, Belnap J, Sparks JP. 2012. Precipitation-driven carbon balance controls survivorship of desert biocrust mosses. Ecology 93:1626–36.CrossRefGoogle Scholar
  16. Couradeau E, Karaoz U, Lim HC, da Rocha UN, Northen T, Brodie E, Garcia-Pichel F. 2016. Bacteria increase arid-land soil surface temperature through the production of sunscreens. Nat Commun 7:10373.CrossRefGoogle Scholar
  17. 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 126:363–78.CrossRefGoogle Scholar
  18. Delgado-Baquerizo M, Maestre FT, Gallardo A, Bowker MA, Wallenstein MD, Quero JL, Ochoa V, Gozalo B, Garcia-Gomez M, Soliveres S, Garcia-Palacios P, Berdugo M, Valencia E, Escolar C, Arredondo T, Barraza-Zepeda C, Bran D, Carreira JA, Chaieb M, Conceicao AA, Derak M, Eldridge DJ, Escudero A, Espinosa CI, Gaitan J, Gatica MG, Gomez-Gonzalez S, Guzman E, Gutierrez JR, Florentino A, Hepper E, Hernandez RM, Huber-Sannwald E, Jankju M, Liu J, Mau RL, Miriti M, Monerris J, Naseri K, Noumi Z, Polo V, Prina A, Pucheta E, Ramirez E, Ramirez-Collantes DA, Romao R, Tighe M, Torres D, Torres-Diaz C, Ungar ED, Val J, Wamiti W, Wang D, Zaady E. 2013. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502:672–6.CrossRefGoogle Scholar
  19. Delgado-Baquerizo M, Gallardo A, Covelo F, Prado-Comesaña A, Ochoa V, Maestre FT. 2015. Differences in thallus chemistry are related to species-specific effects of biocrust-forming lichens on soil nutrients and microbial communities. Funct Ecol 29:1087–98.CrossRefGoogle Scholar
  20. Elbert W, Weber B, Burrows S, Steinkamp J, Budel B, Andreae MO, Poschl U. 2012. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–62.CrossRefGoogle Scholar
  21. Escolar C, Maestre FT, Rey A. 2015. Biocrusts modulate warming and rainfall exclusion effects on soil respiration in a semi-arid grassland. Soil Biol Biochem 80:9–17.CrossRefGoogle Scholar
  22. Ferrenberg S, Faist AM, Howell A, Reed SC. 2017a. Biocrusts enhance soil fertility and Bromus tectorum growth, and interact with warming to influence germination. Plant Soil.  https://doi.org/10.1007/s11104-017-3525-1.Google Scholar
  23. Ferrenberg S, Reed SC, Belnap J. 2015. Climate change and physical disturbance cause similar community shifts in biological soil crusts. Proc Natl Acad Sci 112:12116–21.CrossRefGoogle Scholar
  24. Ferrenberg S, Tucker CL, Reed SC. 2017b. Biological soil crusts: diminutive communities of potential global importance. Fron Ecol Environ 15(3):160–7.CrossRefGoogle Scholar
  25. Fierer N, Craine JM, McLauchlan K, Schimel JP. 2005. Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–6.CrossRefGoogle Scholar
  26. Garcia-Pichel F, Johnson SL, Youngkin D, Belnap J. 2003. Small-scale vertical distribution of bacterial biomass and diversity in biological soil crusts from arid lands in the Colorado Plateau. Microb Ecol 46:312–21.CrossRefGoogle Scholar
  27. Green TA, Proctor MC. 2016. Physiology of photosynthetic organisms within biological soil crusts: their adaptation, flexibility, and plasticity. biological soil crusts: an organizing principle in drylands. Berlin: Springer. pp 347–81.CrossRefGoogle Scholar
  28. 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. Global Change Biol 16:2763–74.CrossRefGoogle Scholar
  29. 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 66:620–34.CrossRefGoogle Scholar
  30. Janssens IA, Kowalski AS, Ceulemans R. 2001. Forest floor CO2 fluxes estimated by eddy covariance and chamber-based model. Agric Forest Meteorol 106:61–9.CrossRefGoogle Scholar
  31. Jasoni RL, Smith SD, Arnone JA. 2005. Net ecosystem CO2 exchange in Mojave Desert shrublands during the eighth year of exposure to elevated CO2. Global Change Biol 11:749–56.CrossRefGoogle Scholar
  32. Kizito F, Campbell CS, Campbell GS, Cobos DR, Teare BL, Carter B, Hopmans JW. 2008. Frequency, electrical conductivity and temperature analysis of a low-cost capacitance soil moisture sensor. J Hydrol 352:367–78.CrossRefGoogle Scholar
  33. Klos PZ, Link TE, Abatzoglou JT. 2014. Extent of the rain-snow transition zone in the western U.S. under historic and projected climate. Geophys Res Lett 41:4560–8.CrossRefGoogle Scholar
  34. Lange O, Belnap J, Lange) O. 2003. Photosynthesis of soil-biota as dependent on environmental factors. Biol Soil Crusts: Struct Funct Manag 349–360.Google Scholar
  35. Lange OL, Green TA, Heber U. 2001. Hydration-dependent photosynthetic production of lichens: what do laboratory studies tell us about field performance? J Exp Bot 52:2033–42.CrossRefGoogle Scholar
  36. Li XR, Zhang P, Su YG, Jia RL. 2012. Carbon fixation by biological soil crusts following revegetation of sand dunes in arid desert regions of China: a four-year field study. Catena 97:119–26.CrossRefGoogle Scholar
  37. Lloyd J, Taylor JA. 1994. On the temperature dependence of soil respiration. Funct Ecol 8:315–23.CrossRefGoogle Scholar
  38. Luo Y, Wan S, Hui D, Wallace LL. 2001. Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–5.CrossRefGoogle Scholar
  39. Maestre FT, Bowker MA, Eldridge DJ, Cortina J, Lázaro R, Gallardo A, Delgado-Baquerizo M, Berdugo M, Castillo-Monroy AP, Valencia E. 2016. Biological soil crusts as a model system in ecology. biological soil crusts: an organizing principle in drylands. Berlin: Springer. pp 407–25.CrossRefGoogle Scholar
  40. Maestre FT, Castillo-Monroy AP, Bowker MA, Ochoa-Hueso R. 2012a. Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. J Ecol 100:317–30.CrossRefGoogle Scholar
  41. Maestre FT, Escolar C, de Guevara ML, 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. Global Change Biol 19:3835–47.CrossRefGoogle Scholar
  42. Maestre FT, Salguero-Gómez R, Quero JL. 2012b. It is getting hotter in here: determining and projecting the impacts of global environmental change on drylands. Philos Trans R Soc Lond B Biol Sci 367(1606):3062–75.CrossRefGoogle Scholar
  43. Marschall M, Proctor MC. 2004. Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Ann Bot 94:593–603.CrossRefGoogle Scholar
  44. 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 5:13767.CrossRefGoogle Scholar
  45. Ogle K, Barber JJ. 2008. Bayesian data—model integration in plant physiological and ecosystem ecology. Progress in botany. Berlin: Springer. pp 281–311.Google Scholar
  46. Pan Z, Pitt WG, Zhang Y, Wu N, Tao Y, Truscott TT. 2016. The upside-down water collection system of Syntrichia caninervis. Nat Plants 2:16076.CrossRefGoogle Scholar
  47. Pendleton RL, Pendleton BK, Howard GL, Warren SD. 2003. Growth and nutrient content of herbaceous seedlings associated with biological soil crusts. Arid Land Res Manag 17:271–81.CrossRefGoogle Scholar
  48. Pointing SB, Belnap J. 2014. Disturbance to desert soil ecosystems contributes to dust-mediated impacts at regional scales. Biodivers Conserv 23:1659–67.CrossRefGoogle Scholar
  49. Poulter B, Frank D, Ciais P, Myneni RB, Andela N, Bi J, Broquet G, Canadell JG, Chevallier F, Liu YY, Running SW, Sitch S, van der Werf GR. 2014. Contribution of semi-arid ecosystems to interannual variability of the global carbon cycle. Nature 509:600–3.CrossRefGoogle Scholar
  50. Raich J, Rastetter E, Melillo J, Kicklighter D, Steudler P, Peterson B, Grace A, Moore B, Vorosmarty C. 1991. Potential net primary productivity in South America: application of a global model. Ecol Appl 1:399–429.CrossRefGoogle Scholar
  51. 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 2:752–5.CrossRefGoogle Scholar
  52. Reed SC, Maestre FT, Ochoa-Hueso R, Kuske CR, Darrouzet-Nardi A, Oliver M, Darby B, Sancho LG, Sinsabaugh RL, Belnap J. 2016. Biocrusts in the Context of Global Change. In: Weber B, Büdel B, Belnap J, Eds. Biological soil crusts: an organizing principle in drylands. Cham: Springer. p 451–76.CrossRefGoogle Scholar
  53. Rey A. 2015. Mind the gap: non-biological processes contributing to soil CO2 efflux. Global Change Biol 21:1752–61.CrossRefGoogle Scholar
  54. 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 7:44188.CrossRefGoogle Scholar
  55. Safriel U, Adeel Z. 2005. Drylands. Chapter 22 of millennium ecosystem assessment. Washington, DC: Island Press.Google Scholar
  56. Sancho LG, Belnap J, Colesie C, Raggio J, Weber B. 2016. Carbon budgets of biological soil crusts at micro-, meso-, and global scales: an organizing principle in drylands. Berlin: Springer. pp 287–304.CrossRefGoogle Scholar
  57. Schimel DS. 2010. Drylands in the earth system. Science 327:418–19.CrossRefGoogle Scholar
  58. Schlesinger WH. 2017. An evaluation of abiotic carbon sinks in deserts. Global Change Biol 23:25–7.CrossRefGoogle Scholar
  59. Schlesinger WH, Belnap J, Marion G. 2009. On carbon sequestration in desert ecosystems. Global Change Biol 15:1488–90.CrossRefGoogle Scholar
  60. Strickland MS, Lauber C, Fierer N, Bradford MA. 2009. Testing the functional significance of microbial community composition. Ecology 90:441–51.CrossRefGoogle Scholar
  61. Thomas AD, Hoon SR, Dougill AJ. 2011. Soil respiration at five sites along the Kalahari transect: effects of temperature, precipitation pulses and biological soil crust cover. Geoderma 167–68:284–94.CrossRefGoogle Scholar
  62. Torres-Cruz TJ, Howell AJ, Reibold RH, McHugh TA, Eickhoff MA, Reed SC. 2018. Species-specific nitrogenase activity in lichen-dominated biological soil crusts from the Colorado Plateau, USA. Plant Soil.  https://doi.org/10.1007/s11104-018-3580-2.Google Scholar
  63. Tucker CL, Bell J, Pendall E, Ogle K. 2013. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Global Change Biol 19:252–63.CrossRefGoogle Scholar
  64. Tucker CL, McHugh TA, Howell A, Gill R, Weber B, Belnap J, Grote E, Reed SC. 2017. The concurrent use of novel soil surface microclimate measurements to evaluate CO2 pulses in biocrusted interspaces in a cool desert ecosystem. Biogeochemistry 135:239–49.CrossRefGoogle Scholar
  65. Tucker CL, Reed SC. 2016. Low soil moisture during hot periods drives apparent negative temperature sensitivity of soil respiration in a dryland ecosystem: a multi-model comparison. Biogeochemistry 128:155–69.CrossRefGoogle Scholar
  66. Weber B, Bowker M, Zhang Y, Belnap J. 2016. Natural recovery of biological soil crusts after disturbance. Biological soil crusts: an organizing principle in drylands. Berlin: Springer. pp 479–98.Google Scholar
  67. 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 112:15384–9.CrossRefGoogle Scholar
  68. Wertin T, Reed S, 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 177:997–1013.CrossRefGoogle Scholar
  69. Wilske B, Burgheimer J, Karnieli A, Zaady E, Andreae M, Yakir D, Kesselmeier J. 2008. The CO 2 exchange of biological soil crusts in a semiarid grass-shrubland at the northern transition zone of the Negev desert, Israel. Biogeosci Discus 5:1969–2001.CrossRefGoogle Scholar
  70. Wilske B, Burgheimer J, Maseyk K, Karnieli A, Zaady E, Andreae M, Yakir D, Kesselmeier J. 2009. Modeling the variability in annual carbon fluxes related to biological soil crusts in a Mediterranean shrubland. Biogeosci Discus 6:7295–324.CrossRefGoogle Scholar
  71. Wohlfahrt G, Fenstermaker LF, Arnone Iii JA. 2008. Large annual net ecosystem CO2 uptake of a Mojave Desert ecosystem. Global Change Biol 14:1475–87.CrossRefGoogle Scholar
  72. Wu L, Zhang YM, Zhang J, Downing A. 2015. Precipitation intensity is the primary driver of moss crust-derived CO2 exchange: Implications for soil C balance in a temperate desert of northwestern China. Eur J Soil Biol 67:27–34.CrossRefGoogle Scholar
  73. Zaady E, Kuhn U, Wilske B, Sandoval-Soto L, Kesselmeier J. 2000. Patterns of CO2 exchange in biological soil crusts of successional age. Soil Biol Biochem 32:959–66.CrossRefGoogle Scholar
  74. Zhang Y, Aradottir AL, Serpe M, Boeken B. 2016. Interactions of biological soil crusts with vascular plants. Biological soil crusts: an organizing principle in drylands. Berlin: Springer. pp 385–406.CrossRefGoogle Scholar
  75. Zhao Y, Zhang ZS, Hu YG, Chen YL. 2016. The seasonal and successional variations of carbon release from biological soil crust-covered soil. J Arid Environ 127:148–53.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature (This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply) 2018

Authors and Affiliations

  • Colin L. Tucker
    • 1
    Email author
  • Scott Ferrenberg
    • 1
    • 2
  • Sasha C. Reed
    • 1
  1. 1.Southwest Biological Science CenterUS Geological SurveyMoabUSA
  2. 2.Department of BiologyNew Mexico State UniversityLas CrucesUSA

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