Abstract
Biological soil crusts (biocrusts) naturally coexist with vascular plants in many dryland ecosystems. Although most studies of dryland biocrusts have been conducted in warm deserts, dryland biocrusts also exist in the Arctic, where they may be an important source of nitrogen (N) and carbon (C) to nutrient-limited environments. In Kangerlussuaq, Greenland, wind-driven soil erosion has created a heterogeneous landscape where biocrusts dominate distinct patches of soil but are absent from the surrounding shrub and graminoid tundra. Prior to this study, little was known about the physical development and nutrient cycling of west Greenland biocrusts and their role in maintaining landscape heterogeneity. We characterized the physical properties, lichen assemblages, and nutrient concentrations of biocrusts and underlying soils along gradients in biocrust development and age. We found that biocrusts took 180 ± 40 years to fully develop and that biocrusts became thicker and soil penetration resistance increased as they developed. The N-fixing lichen Stereocaulon sp. was found throughout the study region at all stages of biocrust development. Natural 15N abundance suggests that Stereocaulon sp. obtains about half of its N from biological fixation and that some biologically fixed N is incorporated into the underlying soils over time. Although the N and C concentrations of underlying soils increased slightly with biocrust development, nutrient concentrations under the most developed biocrusts remained low compared to the surrounding vegetated tundra. Our results suggest that biocrusts are a persistent feature and play an important role in maintaining the high spatial heterogeneity of the Kangerlussuaq terrestrial landscape.
Similar content being viewed by others
References
Anderson NJ, Saros JE, Bullard JE, Cahoon SMP, Mcgowan S, Bagshaw EA, Barry CD, Bindler R, Burpee BT, Carrivick JL, Fowler RA, Fox AD, Fritz SC, Giles ME, Hamerlik L, Ingeman-Nielsen T, Law AC, Mernild SH, Northington RM, Osburn CL, Pla-Rabes S, Post E, Telling J, Stroud DA, Whiteford EJ, Yallop ML, Yde JC. 2017. The arctic in the twenty-first century: changing biogeochemical linkages across a paraglacial landscape of Greenland. Bioscience 67:118–33.
Barger NN, Weber B, Garcia-Pichel F, Zaady E, Belnap J. 2016. Patterns and controls on nitrogen cycling of biological soil crusts. In: Weber B, Büdel B, Belnap J, Eds. Biological soil crusts: an organizing principle in drylands. Berlin: Springer. p 257–85.
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 2:3132–44.
Belnap J, Büdel B. 2016. Biological soil crusts as soil stabilizers. In: Weber B, Büdel B, Belnap J, Eds. Biological soil crusts: an organizing principle in Drylands. Berlin: Springer. p 305–20.
Belnap J, Eldridge DJ. 2003. Disturbance and recovery of biological soil crusts. In: Belnap J, Lange O, Eds. Biological soil crusts: structure, function, and management. Berlin: Springer. p 363–84.
Belnap J, Phillips SL, Witwicki DL, Miller ME. 2008. Visually assessing the level of development and soil surface stability of cyanobacterially dominated biological soil crusts. J Arid Environ 72:1257–64.
Bowker MA. 2007. Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23.
Bradley-Cook JI, Virginia RA. 2016. Soil carbon storage, respiration potential, and organic matter quality across an age and climate gradient in southwestern Greenland. Polar Biol 39:1283–95.
Brankatschk R, Fischer T, Veste M, Zeyer J. 2013. Succession of N cycling processes in biological soil crusts on a Central European inland dune. FEMS Microbiol Ecol 83:149–60.
Breen K, Levesque E. 2006. Proglacial succession of biological soil crusts and vascular plants: biotic interactions in the High Arctic. Can J Bot Rev Can Bot 84:1714–31.
Breen K, Levesque E. 2008. The influence of biological soil crusts on soil characteristics along a High Arctic glacier foreland, Nunavut, Canada. Arct Antarct Alp Res 40:287–97.
Brodo IM, Sharnoff S, Sharnoff SD, Canadian Museum of Nature. 2001. Lichens of North America. New Haven: Yale University Press.
Bullard JE, Austin MJ. 2011. Dust generation on a proglacial floodplain, West Greenland. Aeolian Res 3:43–54.
Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Penuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ. 2009. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–92.
Deines L, Rosentreter R, Eldridge DJ, Serpe MD. 2007. Germination and seedling establishment of two annual grasses on lichen-dominated biological soil crusts. Plant Soil 295:23–35.
Dijkmans JWA, Törnqvist TE. 1991. Modern periglacial eolian deposits and landforms in the Sondre Stromfjord area, West Greenland and their palaeoenvironmental implications. Meddelelser Om Groenl Geosci 25:1–39.
Ellis C, Crittenden P, Scrimgeour C, Ashcroft C. 2003. The natural abundance of N-15 in mat-forming lichens. Oecologia 136:115–23.
Evans R, Ehleringer J. 1993. A break in the nitrogen-cycle in aridlands: evidence from delta-N-15 of soils. Oecologia 94:314–17.
Evans R, Lange O. 2003. Biological soil crusts and ecosystem carbon and nitrogen dynamics. In: Belnap J, Lange O, Eds. Biological soil crusts: structure, function, and management. Berlin: Springer. p 263–80.
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.
Forman SL, Marín L, Van DV, Tremper C, Csatho B. 2007. Little ice age and neoglacial landforms at the Inland Ice margin, Isunguata Sermia, Kangerlussuaq, west Greenland. Boreas 36:341–51.
Guo Y, Zhao H, Zuo X, Drake S, Zhao X. 2008. Biological soil crust development and its topsoil properties in the process of dune stabilization, Inner Mongolia, China. Environ Geol 54:653–62.
Hanna E, Mernild SH, Cappelen J, Steffen K. 2012. Recent warming in Greenland in a long-term instrumental (1881–2012) climatic context: I. Evaluation of surface air temperature records. Environ Res Lett 7:045404.
Hansen E. 2000. A contribution to the lichen flora of the Kangerlussuaq area, West Greenland. Cryptogam Mycol 21:53–9.
Hansen ES. 2001. Lichen-rich soil crusts of Arctic Greenland. In: Belnap J, Lange OL, Eds. Biological Soil Crusts: Structure, Function, and Management. Berlin: Springer. pp 57–65.
Heindel RC, Chipman JW, Dietrich JT, Virginia RA. 2018. Quantifying rates of soil deflation with Structure-from-Motion photogrammetry in west Greenland. Arct Antarct Alp Res 50:SI00012.
Heindel RC, Chipman JW, Virginia RA. 2015. The spatial distribution and ecological impacts of Aeolian soil Erosion in Kangerlussuaq, West Greenland. Ann Assoc Am Geogr 105:875–90.
Heindel RC, Culler LE, Virginia RA. 2017a. Rates and processes of aeolian soil erosion in West Greenland. The Holocene 27:1281–90.
Heindel RC, Culler LE, Virginia RA. 2017b. Data from: rates and processes of aeolian soil erosion in West Greenland. Dryad Digital Repository. https://doi.org/10.5061/dryad.v82g6.
Kobylinski A, Fredeen AL. 2015. Importance of arboreal cyanolichen abundance to nitrogen cycling in sub-boreal spruce and fir forests of Central British Columbia, Canada. Forests 6:2588–607.
Kopec BG, Lauder AM, Posmentier ES, Feng X. 2014. The diel cycle of water vapor in west Greenland. J Geophys Res-Atmospheres 119:9386–99.
Ladrón de Guevara M, 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 23:1787–807.
Langhans TM, Storm C, Schwabe A. 2009. Biological soil crusts and their microenvironment: impact on emergence, survival and establishment of seedlings. Flora 204:157–68.
Levy LB, Kelly MA, Howley JA, Virginia RA. 2012. Age of the Ørkendalen moraines, Kangerlussuaq, Greenland: constraints on the extent of the southwestern margin of the Greenland Ice Sheet during the Holocene. Quat Sci Rev 52:1–5.
Line M. 1992. Nitrogen-fixation in the sub-Antarctic Macquarie Island. Polar Biol 11:601–6.
Mernild SH, Hanna E, McConnell JR, Sigl M, Beckerman AP, Yde JC, Cappelen J, Malmros JK, Steffen K. 2015. Greenland precipitation trends in a long-term instrumental climate context (1890–2012): evaluation of coastal and ice core records. Int J Climatol 35:303–20.
Oulehle F, Rowe EC, Myska O, Chuman T, Evans CD. 2016. Plant functional type affects nitrogen use efficiency in high-Arctic tundra. Soil Biol Biochem 94:19–28.
Rousk K, Sorensen PL, Michelsen A. 2016. Nitrogen transfer from four nitrogen-fixer associations to plants and soils. Ecosystems 19:1491–504.
Russow R, Veste M, Bohme F. 2005. A natural N-15 approach to determine the biological fixation of atmospheric nitrogen by biological soil crusts of the Negev Desert. Rapid Commun Mass Spectrom 19:3451–6.
Sancho LG, Belnap J, Colesie C, Raggio J, Weber B. 2016. Carbon budgets of biological soil crusts at micro-, meso-, and global scales. In: Weber B, Büdel B, Belnap J, Eds. Biological soil crusts: an organizing principle in drylands. Berlin: Springer. p 287–304.
Shearer G, Kohl D. 1986. N-2-fixation in field settings—estimations based on natural N-15 abundance. Aust J Plant Physiol 13:699–756.
Stewart KJ, Coxson D, Grogan P. 2011a. Nitrogen inputs by associative cyanobacteria across a low Arctic Tundra landscape. Arct Antarct Alp Res 43:267–78.
Stewart KJ, Lamb EG, Coxson DS, Siciliano SD. 2011b. Bryophyte-cyanobacterial associations as a key factor in N-2-fixation across the Canadian Arctic. Plant Soil 344:335–46.
Ten Brink NW, Weidick A. 1974. Greenland ice sheet history since the last glaciation. Quat Res 4:429–40.
Thomas AD, Dougill AJ. 2007. Spatial and temporal distribution of cyanobacterial soil crusts in the Kalahari: implications for soil surface properties. Geomorphology 85:17–29.
Urbanowicz C, Virginia RA, Irwin RE. 2017. The response of pollen-transport networks to landscape-scale climate variation. Polar Biol 40:2253–63.
Weber B, Bowker MA, Zhang Y, Belnap J. 2016a. Natural recovery of biological soil crusts after disturbance. In: Weber B, Büdel B, Belnap J, Eds. Biological soil crusts: an organizing principle in drylands. Berlin: Springer. p 479–98.
Weber B, Büdel B, Belnap J. 2016b. Biological soil crusts: an organizing principle in Drylands. Berlin: Springer.
Yoshitake S, Uchida M, Koizumi H, Kanda H, Nakatsubo T. 2010. Production of biological soil crusts in the early stage of primary succession on a High Arctic glacier foreland. New Phytol 186:451–60.
Zhang Y, Nie H. 2011. Effects of biological soil crusts on seedling growth and element uptake in five desert plants in Junggar Basin, western China. Chin J Plant Ecol 35:380–8.
Acknowledgements
We thank Robbie Score and the staff of CH2M Hill Polar Field Services for their logistics and field support in Kangerlussuaq, Greenland. Becca Novello and Phoebe Racine helped collect samples, Kristin Winkle processed soil samples with funding through the Dartmouth Women in Science Project (WISP), Paul Zietz (Dartmouth Environmental Measurements Lab) conducted the total C and N analyses, and Lee McDavid (Dartmouth Institute of Arctic Studies) provided administrative support. A special thanks to Troy McMullin and Irwin Brodo at the Canadian Museum of Nature for lichen species identification. This work was supported by the National Science Foundation Office of Polar Programs [grant numbers 0801490 and 1506155 to RAV]. FCG was funded by a Sophomore Science Scholarship through Dartmouth Undergraduate Advising & Research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Author contributions
RCH, AMS, and RAV designed the study. FCG and AMS developed methods. RCH, FCG, and AMS collected data. RCH analyzed data and wrote early drafts of the manuscript. All authors contributed significantly to manuscript revisions.
Rights and permissions
About this article
Cite this article
Heindel, R.C., Governali, F.C., Spickard, A.M. et al. The Role of Biological Soil Crusts in Nitrogen Cycling and Soil Stabilization in Kangerlussuaq, West Greenland. Ecosystems 22, 243–256 (2019). https://doi.org/10.1007/s10021-018-0267-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-018-0267-8