Biocrust carbon isotope signature was depleted under a C3 forb compared to interspace

Regular Article



Plants and biological soil crusts (biocrusts) are the key producers in drylands, but biocrusts seldom show net CO2 uptake. I hypothesized that biocrusts could augment CO2 fixation by incorporating plant-derived carbon.


I collected biocrusts located at the base of Gutierrezia sarothrae (C3 forb), Bouteloua gracilis (C4 grass), and from bare interspaces between plants, and from a mesocosm experiment with live B. gracilis or dead B. gracilis roots. To trace carbon sources, I determined 13C values of the biocrust community, isolated cyanobacteria and lichen, and plant leaves because the photosynthetic pathway distinguishes the tissue 13C values.


Biocrust communities and washed cyanobacteria and cyanolichen in G. sarothrae microsites were depleted by ~2‰ relative to other locations. Biocrust δ13C did not differ between the interspace and live or dead B. gracilis.


Potential mechanisms for the trend in biocrust δ13C adjacent to C3 plants include differences in microsite conditions, biocrust communities, use of respired CO2 in the soil matrix for photosynthesis, or mixotrophic use of plant photosynthates. Further investigation of this observation may improve understanding of the degree to which the activities of dryland primary producers are coupled.


Biological soil crust C3 plant C4 plant Delta 13Carbon dynamics 



Jenn Rudgers, Bob Sinsabaugh, Lee Taylor, Matt Bowker, and four anonymous reviewers provided valuable manuscript feedback. This project originated as a project funded by Zack Sharp’s Stable Isotope Biogeochemistry course and I received feedback from Dr. Sharp and the other students in the course. Viorel Atudorei and Laura Burkemper provided assistance with sample preparation and processing. The Sevilleta Long Term Ecological Research site (NSF DEB #1440478) and Sevilleta Field Station provided logistic support for sampling. I thank my dad, Creighton Robinson, for letting me sample on his property. Manuscript was prepared with support from NSF DEB DDIG#1557135 and NSF DEB #1557135.

Supplementary material

11104_2017_3558_MOESM1_ESM.docx (81 kb)
ESM 1 (DOCX 81.0 kb)


  1. Ahlstrom A, Raupach MR, Schurgers G, Schurgers G, Smith B, Arneth A, Jung M, Reichstein M, Canadell JG, Friedlingstein P, Jain AK, Kato E, Pulter 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 348:895–899CrossRefPubMedGoogle Scholar
  2. Amundson ARG, Chadwick OA, Sowers JM (1989) A comparison of soil climate and biological activity along an elevation gradient in the eastern Mojave Desert. Oecologia 80:395–400CrossRefPubMedGoogle Scholar
  3. Aranibar JN, Anderson IC, Ringrose S, Macko SA (2003) Importance of nitrogen fixation in soil crusts of southern African arid ecosystems: acetylene reduction and stable isotope studies. J Arid Environ 54:345–358CrossRefGoogle Scholar
  4. Austin AT, Ballaré CL (2010) Dual role of lignin in plant litter decomposition in terrestrial ecosystems. Proc Natl Acad Sci 107:4618–4622CrossRefPubMedPubMedCentralGoogle Scholar
  5. Badger MR, Price GD (1992) The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol Plant 84:606–615CrossRefGoogle Scholar
  6. Bai E, Boutton TW, Liu F, Archer SI (2012) Spatial patterns of soil d13C reveal grassland-to-woodland successional processes. Org Geochem 42:1512–1518CrossRefGoogle Scholar
  7. Beck A, Mayr C (2012) Nitrogen and carbon isotope variability in the green-algal lichen Xanthoria parietina and their implications on mycobiont-photobiont interactions. Ecol Evol 2:3132–3144CrossRefPubMedPubMedCentralGoogle Scholar
  8. Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah. USA Biol Fertil Soils 35:128–135CrossRefGoogle Scholar
  9. Belnap J, Budel B, Lange OL (2001) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin/HeidelbergGoogle Scholar
  10. Benner R, Fogel M, Sprague EK, Hodson RE (1987) Depletion of 13C in lignin and its implications for stable carbon isotope studies. Nature 329:708–710CrossRefGoogle Scholar
  11. 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
  12. Bowker MA, Belnap J, Davidson DW, Goldstein H (2006) Correlates of biological soil crust abundance across a continuum of spatial scales: support for a hierarchical conceptual model. J Appl Ecol 43:152–163CrossRefGoogle Scholar
  13. Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40CrossRefPubMedGoogle Scholar
  14. 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 116:1–17Google Scholar
  15. Brandt LA, King JY, Hobbie SE, Milchunas DG, Sinsabaugh RL (2010) The role of photodegradation in surface litter decomposition across a grassland ecosystem precipitation gradient. Ecosystems 13:765–781CrossRefGoogle Scholar
  16. Breecker DO, Sharp ZD, McFadden LD (2009) Seasonal bias in the formation and stable isotopic composition of pedogenic carbonate in modern soils from central New Mexico. USA Bull Geol Soc Am 121:630–640CrossRefGoogle Scholar
  17. Breecker DO, Bergel S, Nadel M, Tremblay MM, Osuna-Orozco R, Larson TE, Sharp ZD (2015) Minor stable carbon isotope fractionation between respired carbon dioxide and bulk osil organic matter during laboratory incubation of topsoil. Biogeochem 123:83–90CrossRefGoogle Scholar
  18. Brüggemann N, Gessler A, Kayler Z, Keel SG, Badeck F, Barthel M, Boeckx P, Buchmann N, Brugnoli E, Esperschutz J, Gavrichkova O, Ghashghaie J, Gomez-Casanovas N, Keitel C, Knohl A, Kuptz D, Palacio S, Salmon Y, Uchida Y, Bahn M (2011) Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review. Biogeosciences 8:3457–3489CrossRefGoogle Scholar
  19. Cable JM, Huxman TE (2004) Precipitation pulse size effects on Sonoran Desert soil microbial crusts. Oecologia 141:317–324CrossRefPubMedGoogle Scholar
  20. Connin SL, Feng X, Virginia RA (2001) Isotopic discrimination during long-term decomposition in an arid land ecosystem. Soil Biol Biochem 33:41–51CrossRefGoogle Scholar
  21. Cuna S, Balas G, Hauer E (2007) Effects of natural environmental factors on delta13C of lichens. Isot Environ Health Stud 43:95–104CrossRefGoogle Scholar
  22. Darby BJ, Neher DA (2012) Stable isotope composition of microfauna supports the occurrence of biologically fixed nitrogen from cyanobacteria in desert soil food webs. J Arid Environ 85:76–78CrossRefGoogle Scholar
  23. 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 126:363–378CrossRefGoogle Scholar
  24. de Guevara ML, Lázaro R, Quero JL, Ochoa V, Gozalo B, Berdugo M, Uclés 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
  25. Dumig A, Rumpel C, Dignac MF, Kogel-Knabner I (2013) The role of lignin for the delta13C signature in C4 grassland and C3 forest soils. Soil Biol Biochem 57:1–13CrossRefGoogle Scholar
  26. 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
  27. Fernandez I, Mahieu N, Cadisch G (2003) Carbon isotopic fractionation during decomposition of plant materials of different quality. Glob Biogeochem Cycles 17:1075CrossRefGoogle Scholar
  28. 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 340:1574–1577CrossRefPubMedGoogle Scholar
  29. Green LE, Porras-Alfaro A, Sinsabaugh RL (2008) Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. J Ecol 96:1076–1085CrossRefGoogle Scholar
  30. Gustavs L, Schumann R, Karsten U, Lorenz M (2016) Mixotrophy in the terrestrial green alga Apatococcus lobatus Trebouxiophyceae. Chlorophyta J Phycol 52:311–314CrossRefPubMedGoogle Scholar
  31. Harris D, Horwáth WR, van Kessel C (2001) Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon-13 isotopic analysis. Soil Sci Soc Am J 65:1853–1856CrossRefGoogle Scholar
  32. Hinga KR, Arthur MA, Pilson MEQ, Whitaker D (1994) Carbon isotope fractionation by marine phytoplankton in culture: the effects of CO2 concentration, pH, temperature, and species. Glob Biochem Cycles 8:91–102CrossRefGoogle Scholar
  33. Hobbie EA, Werner RA (2004) Bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytol 161:371–385CrossRefGoogle Scholar
  34. Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–268CrossRefPubMedGoogle Scholar
  35. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480CrossRefGoogle Scholar
  36. Kattge J, Diaz S, Lavorel S, Prentice IC, Leadley P, Bonisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, Violle C, Harrison SP, Van Bodegom PM, Reichstein M, Enquist BJ, Soudzilovskaia NA, Ackerly DD, Anand M, Atkin O, Bahn M, Baker TR, Baldocchi D, Bekker R, Blanco CC, Blonder B, Bond WJ, Bradstock R, Bunker DE, Casanoves F, Cavender-Bares J, Chambers JQ, Chapin FS, Chave J, Coomes D, Cornwell WK, Craine JM, Dobrin BH, Duarte L, Durka W, Elser J, Esser G, Estiarte M, Fagan WF, Fang J, Fernandez-Mendez F, Fidelis A, Finegan B, Flores O, Ford H, Frank D, Freschet GT, Fyllas NM, Gallagher RV, Green WA, Gutierrez AG, Hickler T, Higgins SI, Hodgson JG, Jalili A, Jansen S, Joly CA, Kerkhoff AJ, Kirkup D, Kitajima K, Kleyer M, Klotz S, Knops JMH, Kramer K, Kuhn I, Kurokawa H, Laughlin D, Lee TD, Leishman M, Lens F, Lenz T, Lewis SL, Lloyd J, Llusia J, Louault F, Ma S, Mahecha MD, Manning P, Massad T, Medlyn BE, Messier J, Moles AT, Muller SC, Nadrowski K, Naeem S, Niinemets U, Nollert S, Nuske A, Ogaya R, Oleksyn J, Onipchenko VG, Onoda Y, Ordonez J, Overbeck G, Ozinga WA, Patino S, Paula S, Pausas JG, Penuelas J, Phillips OL, Pillar V, Poorter H, Poorter L, Poschlod P, Prinzing A, Proulx R, Rammig A, Reinsch S, Reu B, Sack L, Salgado-Negret B, Sardans J, Shiodera S, Shipley B, Siefert A, Sosinski E, Soussana JF, Swaine E, Swenson N, Thompson K, Thornton P, Waldram M, Weiher E, White M, White S, Wright SJ, Yguel B, Zaehle S, Zanne AE, Wirth C (2011) TRY - a global database of plant traits. Glob Chang Biol 17:2905–2935CrossRefPubMedCentralGoogle Scholar
  37. Keeling R F, Piper S C, Bollenbacher A F, and Walker S J 2010 Monthly atmospheric 13C/12C isotopic ratios for 11 SIO stations. In Trends: A Compendium of Data on Global Change. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tenn, U.S.A.Google Scholar
  38. Kieft TL, White CS, Loftin SR, Aguilar R, Craig JA, Skaar DA (1998) Temporal dynamics in soil carbon and nitrogen resources at a grassland-shrubland ecotone. Ecology 79:671–683Google Scholar
  39. Kuske CR, Ticknor LO, Miller ME, Dunbar JM, Davis JA, Barns SM, Belnap J (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an arid grassland. Appl Environ Microbiol 68:1854–1863CrossRefPubMedPubMedCentralGoogle Scholar
  40. Milchunas DG, Lee CA, Laurenroth WK, Coffin DP (1992) A comparison of 14C, 86Rb, and total excavation for determination of root distributions of individual plants. Plant Soil 144:125–132CrossRefGoogle Scholar
  41. Moore D I (2016) Meteorology Data from the Sevilleta National Wildlife Refuge, New Mexico 1988- present Dataset. Accessed 15 May 2016
  42. Mun HT, Whitford WG (1998) Changes in mass and chemistry of plant roots during long-term decomposition on a Chihuahuan Desert watershed. Biol Fertil Soils 26:16–22CrossRefGoogle Scholar
  43. Murphy KL, Klopatek JM, Klopatec CC (1998) The effects of litter quality and climate on decomposition along an elevational gradient. Ecol Appl 8:1061–1071CrossRefGoogle Scholar
  44. O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336CrossRefGoogle Scholar
  45. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partioning using stable isotopes: coping with too much variation. PLoS One 5:e9672CrossRefPubMedPubMedCentralGoogle Scholar
  46. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  47. Prǎvǎlie R (2016) Drylands extent and environmental issues: a global approach. Earth-Science Rev 161:259–278CrossRefGoogle Scholar
  48. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  49. Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos Trans R Soc Lond Ser B Biol Sci 363:2641–2650CrossRefGoogle Scholar
  50. Schlesinger WH, Pilmanis AM (1998) Plant-soil interactions in deserts. Biogeochemistry 42:169–187CrossRefGoogle Scholar
  51. Sponseller RA (2007) Precipitation pulses and soil CO2 flux in a Sonoran Desert ecosystem. Glob Chang Biol 13:426–436CrossRefGoogle Scholar
  52. Steven B, Gallegos-Graves LV, Yeager C, Belnap J, Kuske CA (2014) Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils. Soil Biol Biochem 69:302–312CrossRefGoogle Scholar
  53. Tiunov AV (2007) Stable isotopes of carbon and nitrogen in soil ecological studies. Biol Bull 34:395–407CrossRefGoogle Scholar
  54. Vuorio K, Meili M, Sarvala J (2006) Taxon-specific variation in the stable isotopic signatures d13C and d15N of lake phytoplankton. Freshw Biol 51:807–822CrossRefGoogle Scholar
  55. Wada E, Ohki K, Yoshikawa S, Parker PL, Van Baalen C, Matsumoto GI, Aita MN, Saino T (2012) Ecological aspects of carbon and nitrogen isotope ratios of cyanobacteria. Plankt Benthos Res 7:135–145CrossRefGoogle Scholar
  56. Wang C, Liu D, Luo W, Fang Y, Wang X, Lü X, Jiang Y, Hang X, Bai E (2016) Variations in leaf carbon isotope composition along an arid and semi-arid grassland transect in Northern China. J Plant Ecol 9:1–10Google Scholar
  57. Wedin DA, Tieszen LL, Dewey B, Pastor J (1995) Carbon isotope dynamics during grass decomposition and soil organic matter formation. Ecology 76:1383–1392CrossRefGoogle Scholar
  58. Werth M, Kuzyakov Y (2010) 13C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42:1372–1384CrossRefGoogle Scholar
  59. Western Regional Climate Center (2015) Local Climate Data Summaries. Accessed 31 Dec 2015
  60. Wilske B, Burgheimer J, Karnieli A, Zaady E, Andreae MO, Yakir D, Kesselmeier J (2008) The CO2 exchange of biological soil crusts in a semiarid grass-shrubland at the northern transition zone of the Negev desert, Israel. Biogeosciences 5:1411–1423CrossRefGoogle Scholar
  61. Yang W, Magid J, Christensen S, Ronn R, Ambus P, Ekelund F (2014) Biological 12C-13C fractionation increases with increasing community-complexity in soil microcosms. Soil Biol Biochem 69:197–201CrossRefGoogle Scholar
  62. Yu H, Jia S, Dai Y (2009) Growth characteristics of the cyanobacterium Nostoc Flagelliforme in photoautotrophic, mixotrophic and heterotrophic cultivation. J Appl Phycol 21:127–133CrossRefGoogle Scholar
  63. 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
  64. Zhou T, Yu R, Li H, Wang B (2008) Ocean forcing to changes in global monsoon precipitation over the recent half-century. J Clim 21:3833–3852CrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.University of New MexicoAlbuquerqueUSA

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