Evidence for phosphorus limitation in high-elevation unvegetated soils, Niwot Ridge, Colorado

  • Clifton P. Bueno de Mesquita
  • Laurel M. Brigham
  • Pacifica Sommers
  • Dorota L. Porazinska
  • Emily C. Farrer
  • John L. Darcy
  • Katharine N. Suding
  • Steven K. SchmidtEmail author


A key challenge to understanding the effects of climate change and nutrient deposition on ecosystem functioning is our lack of knowledge about nutrient limitations of heterotrophic and phototrophic microbial communities. This is especially true in high elevation ecosystems where it has been shown that earlier melt-out of snow beds and glacial retreat is allowing photosynthetic microbes and plants to move into previously unvegetated areas. We used landscape-level analyses of microbial enzyme stoichiometries combined with soil microcosm fertilization studies to determine which nutrients are limiting to microbes in plant-free or sparsely vegetated, snow bed areas of the Colorado Front Range. Both of these independent approaches indicated that the ultimate limiting nutrient in unvegetated and sparsely vegetated soils is phosphorus (P) for phototrophic microbes, with co-limitation by carbon (C) for the entire microbial community. In contrast, vegetated soils in the same watersheds showed more balanced nitrogen (N), P and C co-limitation similar to patterns seen in other plant-dominated ecosystems. In microcosm experiments, P additions resulted in increased growth rates and percent cover by phototrophs, whereas N additions decreased the relative abundances of phototrophs. Taken together, our findings indicate that the colonization of high elevation ecosystems being impacted by N deposition and climate warming will likely be constrained by P limitation of both heterotrophic and phototrophic microbes and by negative impacts of N on microbial phototrophs. These effects may in turn limit the ability of these fragile ecosystems to immobilize inputs of atmospheric N causing increased runoff of excess N to downstream ecosystems.


Cyanobacteria Extreme environments Glacial retreat High-elevation soils Microbial community assembly Microbial succession Phosphorus limitation 



We thank A.J. King, J.G. Smith, S.A. Sartwell, J. Anderson Huxley, M.J. Spasojevic, C.T. White, A.F. Meyer, S.P. O’Neill, B. Todd, and M. Weintraub for field and laboratory assistance.


Funding was provided by NSF grants for studying microbial community assembly and plant migration to higher elevations (DEB-1258160, DEB-1457827 and DEB-1637686), and the Niwot Ridge LTER program (DEB-1027341). Logistical support was provided by the CU Mountain Research Station and Niwot Ridge LTER program.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


  1. Allgeier JE, Rosemond AD, Layman CA (2011) The frequency and magnitude of non-additive responses to multiple nutrient enrichment. J Appl Ecol 48:96–101CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Baron J, Rueth H, Wolfe A et al (2000) Ecosystem responses to nitrogen deposition in the Colorado Front Range. Ecosystems 3:352–368CrossRefGoogle Scholar
  4. Bowman WD, Schardt JC, Schmidt SK (1996) Symbiotic N2 fixation in alpine tundra: ecosystem input and variation in fixation rates among communities. Oecologia 108:345–350CrossRefGoogle Scholar
  5. Bowman WD, Gartner JL, Holland K, Wiedermann M (2006) Nitrogen critical loads for alpine vegetation and terrestrial ecosystem response: are we there yet? Ecol Appl 16:1183–1193CrossRefGoogle Scholar
  6. Bowman WD, Ammad A, Bueno de Mesquita CP, Fierer N, Potter TS, Sternagel S (2018) Limited ecosystem recovery from simulated chronic nitrogen deposition. Ecol Appl 28(7):1762–1772CrossRefGoogle Scholar
  7. Bueno de Mesquita CP, Knelman JE, King AJ et al (2017) Plant colonization of moss-dominated soils in the alpine: microbial and biogeochemical implications. Soil Biol Biochem 111:135–142. CrossRefGoogle Scholar
  8. Bueno de Mesquita CP, Tillmann LS, Bernard CD et al (2018) Topographic heterogeneity explains patterns of vegetation response to climate change (1972–2008) across a mountain landscape, Niwot Ridge, Colorado. Arct Antarct Alp Res 50:e1504492. CrossRefGoogle Scholar
  9. Caine N (2010) Recent hydrologic change in a Colorado alpine basin: an indicator of permafrost thaw? Ann Glaciol 51:130–134CrossRefGoogle Scholar
  10. Caine T (2018) Stream water chemistry data for Albion site, 1982—ongoing. Environmental Data Initiative. Accessed 6 Dec 2019
  11. Caporaso JG, Kuczynski J, Bittinger K, Bushman FD, Costello EK, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  12. Chapin FS III, Walker LR, Fastie C, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175CrossRefGoogle Scholar
  13. Cross WF, Hood JM, Benstead JP, Huryn AD, Nelson D (2015) Interactions between temperature and nutrients across levels of ecological organization. Glob Change Biol 21:1025–1040CrossRefGoogle Scholar
  14. Darcy JL, Schmidt SK (2016) Nutrient limitation of microbial phototrophs on a debris-covered glacier. Soil Biol Biochem 95:156–163CrossRefGoogle Scholar
  15. Darcy JL, Schmidt SK, Knelman JE, Cleveland CC, Castle SC, Nemergut DR (2018) Phosphorus, not nitrogen, limits plants and microbial primary producers following glacial retreat. Science Adv 4:eaaq0942CrossRefGoogle Scholar
  16. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microb 72:5069–5072CrossRefGoogle Scholar
  17. Dullinger S, Gattringer A, Thuiller W et al (2012) Extinction debt of high-mountain plants under twenty-first-century climate change. Nat Clim Change 2:619–622. CrossRefGoogle Scholar
  18. Engler R, Randin CF, Thuiller W et al (2011) 21st century climate change threatens mountain flora unequally across Europe. Glob Change Biol 17:2330–2341. CrossRefGoogle Scholar
  19. Erickson TA, Williams MW, Winstral A (2005) Persistence of topographic controls on the spatial distribution of snow in rugged mountain terrain, Colorado, United States. Water Resour Res 41:W04014CrossRefGoogle Scholar
  20. Farrer EC, Ashton IW, Spasojevic MJ et al (2015) Indirect effects of global change accumulate to alter plant diversity but not ecosystem function in alpine tundra. J Ecol 103:351–360. CrossRefGoogle Scholar
  21. Field A, Miles J, Field Z (2012) Discovering statistics using R. SAGE Publications, LondonGoogle Scholar
  22. Fisk MC, Schmidt SK (1996) Microbial responses to nitrogen additions in alpine tundra soils. Soil Biol Biochem 28:751–755CrossRefGoogle Scholar
  23. Freeman KR, Martin AP, Karki D et al (2009a) Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Nat Acad Sci 106:18315–18320CrossRefGoogle Scholar
  24. Freeman KR, Pescador MY, Reed SC et al (2009b) Soil CO2 flux and photoautotrophic community composition in high-elevation, “barren” soils. Environ Microbiol 11:674–686CrossRefGoogle Scholar
  25. Gendron EMS, Darcy JL, Hell K, Schmidt SK (2019) Structure of bacterial and eukaryote communities reflect in situ controls on community assembly in a high-alpine lake. J Microbiol. CrossRefGoogle Scholar
  26. Hill BH, Elonen CM, Seifert LR, May AA, Tarquino E (2012) Microbial enzyme stoichiometry and nutrient limitation in US streams and rivers. Ecol Indic 18:540–551CrossRefGoogle Scholar
  27. Jiang Y, Lei Y, Qin W, Korpelainen H, Li C (2019) Revealing microbial processes and nutrient limitation in soil through ecoenzymatic stoichiometry and glomalin-related soil proteins in a retreating glacier forefield. Geoderma 338:313–324CrossRefGoogle Scholar
  28. Oksanen J, Blanchet FG, Kindt R, et al. (2013) Vegan: community ecology package. R Package Version 2.0-10.
  29. King AJ, Meyer AF, Schmidt SK (2008) High levels of microbial biomass and activity in unvegetated tropical and temperate alpine soils. Soil Biol Biochem 40:2605–2610CrossRefGoogle Scholar
  30. King AJ, Freeman KR, McCormick KF, Lozupone CA, Knight R, Schmidt SK (2010) Biogeography and habitat modelling of high-alpine bacteria. Nat Commun 1:53. CrossRefGoogle Scholar
  31. King AJ, Farrer EC, Suding KN, Schmidt SK (2012) Co-occurrence patterns of plants and soil bacteria in the high-alpine subnival zone track environmental harshness. Front Microbiol. CrossRefGoogle Scholar
  32. Knelman JE, Schmidt SK, Darcy JL et al (2014) Nutrient addition dramatically accelerates microbial community succession. PLoS ONE 9:e102609CrossRefGoogle Scholar
  33. Knowles N, Dettinger MD, Cayan DR (2006) Trends in snowfall versus rainfall in the Western United States. J Clim 19:4545–45559CrossRefGoogle Scholar
  34. Lambers H, Bishop JG, Hopper SD, Laliberté E, Zúñiga-Feest A (2012) Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems. Ann Bot 110(2):329–348CrossRefGoogle Scholar
  35. Ley RE, Schmidt SK (2002) Fungal and bacterial responses to phenolic compounds and amino acids in high altitude barren soils. Soil Biol Biochem 34:989–995CrossRefGoogle Scholar
  36. Ley RE, Williams MW, Schmidt SK (2004) Microbial population dynamics in an extreme environment: controlling factors in talus soils at 3750 m in the Colorado Rocky Mountains. Biogeochemistry 68:313–335CrossRefGoogle Scholar
  37. Li Y, Niu S, Yu G (2016) Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis. Glob Change Biol 22:934–943CrossRefGoogle Scholar
  38. Litaor I, Suding K, Anderson SP, Litus G, Caine N (2018) Alpine catena response to nitrogen deposition and its effect of the aquatic system. Catena 170:108–118CrossRefGoogle Scholar
  39. Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative ß diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73(5):1576–1585CrossRefGoogle Scholar
  40. Mladenov N, Williams MW, Schmidt SK, Cawley K (2012) Atmospheric deposition as a source of carbon and nutrients to an alpine catchment of the Colorado Rocky Mountains. Biogeosciences 9:3337–3355CrossRefGoogle Scholar
  41. Mullen RB, Schmidt SK (1993) Mycorrhizal infection, phosphorus uptake, and phenology in Ranunculus adoneus, implications for the functioning of mycorrhizae in alpine systems. Oecologia 94:229–234CrossRefGoogle Scholar
  42. Nanus L, Williams MW, Campbell DH et al (2008) Evaluating regional patterns in nitrate sources to watersheds in national parks of the Rocky Mountains using nitrate isotopes. Environ Sci Technol 42:6487–6493CrossRefGoogle Scholar
  43. Neff JC, Ballantyne AP, Farmer GL et al (2008) Increasing eolian dust deposition in the western United States linked to human activity. Nat Geosci 1:189–195CrossRefGoogle Scholar
  44. Nemergut DR, Anderson SP, Cleveland CC et al (2007) Microbial community succession in unvegetated, recently-deglaciated soils. Microb Ecol 53:110–122CrossRefGoogle Scholar
  45. Nemergut DR, Townsend AR, Sattin SR et al (2008) The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ Microbiol 10:3093–3105CrossRefGoogle Scholar
  46. Nemergut DR, Cleveland CC, Wieder WR et al (2010) Plot-scale manipulations of organic matter inputs to soils correlate with shifts in microbial community composition in a lowland tropical rain forest. Soil Biol Biochem 42:2153–2160CrossRefGoogle Scholar
  47. Pauli H, Gottfried M, Dullinger S et al (2012) Recent plant diversity changes on Europe’s mountain summits. Science 336:353–355CrossRefGoogle Scholar
  48. Peace WJH, Grubb PJ (1982) Interaction of light and mineral nutrient supply in the growth of impatiens parviflora. New Phytol 90(1):127–150CrossRefGoogle Scholar
  49. Porazinska DL, Farrer EC, Spasojevic MJ, Bueno de Mesquita CP, Sartwell SA, Smith JG, White CT, King AJ, Suding KN, Schmidt SK (2018) Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem. Ecology 99(9):1942–1952CrossRefGoogle Scholar
  50. Ramirez KS, Lauber CL, Knight R et al (2010) Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology 91:3414–3463. CrossRefGoogle Scholar
  51. Recena R, Torrent J, Carmen del Campillo M, Delgado A (2015) Accuracy of Olsen P to assess plant P uptake in relation to soil properties and P forms. Agron Sustain Dev 35:1571–1579CrossRefGoogle Scholar
  52. Schmidt SK, Lipson DA, Ley RE, Fisk MC, West AE (2004) Impacts of chronic nitrogen additions vary seasonally and by microbial functional group in tundra soils. Biogeochemistry 69:1–17CrossRefGoogle Scholar
  53. Schmidt SK, Reed SC, Nemergut DR et al (2008) The earliest stages of ecosystem succession in high-elevation, recently de-glaciated soils. Proc R Soc B 275:2793–2802CrossRefGoogle Scholar
  54. Schmidt SK, Wilson KL, Monson RK, Lipson DA (2009) Exponential growth of snow molds at sub-zero temperatures: an explanation for high beneath-snow respiration rates and Q10 values. Biogeochemistry 95:13–21CrossRefGoogle Scholar
  55. Schmidt SK, Cleveland CC, Nemergut DR et al (2011) Estimating phosphorus availability for microbial growth in an emerging landscape. Geoderma 163:135–140CrossRefGoogle Scholar
  56. Schmidt SK, Nemergut DR, Todd BT, Darcy JL, Cleveland CC, King AJ (2012) A simple method for determining limiting nutrients for photosynthetic crusts. Plant Ecol Divers 5:513–519CrossRefGoogle Scholar
  57. Schmidt SK, Porazinska D, Concienne BL, Darcy JL, King AJ, Nemergut DR (2016) Biogeochemical stoichiometry reveals P and N limitation across the post-glacial landscape of Denali National Park, Alaska. Ecosystems. CrossRefGoogle Scholar
  58. Seastedt TR, Bowman WD, Caine N, McKnight DM, Townsend A, Williams MW (2004) The landscape continuum: a model for high-elevation ecosystems. Bioscience 54:111–121CrossRefGoogle Scholar
  59. Sinsabaugh RL, Hill BH, Folstad-Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic matter acquisition in soil and sediment. Nature 462:795–798CrossRefGoogle Scholar
  60. Suding KN, Ashton IW, Bechtold H, Bowman WD, Mobley ML, Winkleman R (2008) Plant and microbe contribution to community resilience in a directionally changing environment. Ecol Monogr 78:313–329CrossRefGoogle Scholar
  61. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing. ISBN 3-900051-07-0Google Scholar
  62. Vaughan D, Comiso JC, Allison I, Carrasco J, Kaser G, Kwok R, Mote P (2013) Observations: cryosphere. In: Climate Change 2013: the Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the IPCC. Cambridge University Press, CambridgeGoogle Scholar
  63. Vitousek PM (2004) Nutrient cycling and limitation: Hawai’i as a model system. Princeton University Press, PrincetonCrossRefGoogle Scholar
  64. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  65. Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117(1):101e113. CrossRefGoogle Scholar
  66. Weintraub MN, Scott-Denton LE, Schmidt SK, Monson RK (2007) The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem. Oecologia 154:327–338CrossRefGoogle Scholar
  67. Wilcox RR, Schönbrodt FD (2014) The WRS package for robust statistics in R (version 0.24). Retrieved from
  68. Williams MW, Baron JS, Caine N, Sommerfeld R, Sanford R (1996) Nitrogen saturation in the Rocky Mountains. Environ Sci Technol 30:640–646CrossRefGoogle Scholar
  69. Williams MW, Hood E, Molotch N, Caine N, Cowie R, Liu F (2015) The ‘teflon basin’ myth: hydrology and hydrochemistry of a seasonally snow-covered catchment. Plant Ecol Divers 8:639–661CrossRefGoogle Scholar
  70. Yuan X, Knelman JE, Gasarch E, Wang D, Nemergut DR, Seastedt TR (2016) Plant community and soil chemistry responses to long-term nitrogen inputs drive changes in alpine bacterial communities. Ecology 97(6):1543–1554CrossRefGoogle Scholar
  71. Zeglin LH, Sinsabaugh RL, Barrett JE, Gooseff MN, Takacs-Vesbach CD (2009) Landscape distribution of microbial activity in the McMurdo Dry Valleys, linked biotic processes, hydrology, and geochemistry in a cold desert ecosystem. Ecosystems 12:562–573CrossRefGoogle Scholar
  72. Zeng J, Liu X, Song L, Lin X, Zhang H, Shen C, Chu H (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Clifton P. Bueno de Mesquita
    • 1
    • 2
  • Laurel M. Brigham
    • 1
    • 2
  • Pacifica Sommers
    • 1
  • Dorota L. Porazinska
    • 3
  • Emily C. Farrer
    • 4
  • John L. Darcy
    • 5
  • Katharine N. Suding
    • 1
    • 2
  • Steven K. Schmidt
    • 1
    Email author
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  2. 2.Institute of Arctic and Alpine ResearchUniversity of ColoradoBoulderUSA
  3. 3.Department of Entomology and NematologyUniversity of FloridaGainesvilleUSA
  4. 4.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA
  5. 5.Division of Biomedical Informatics and Personalized Medicine, School of MedicineUniversity of Colorado Denver Anschutz Medical CampusAuroraUSA

Personalised recommendations