, Volume 14, Issue 5, pp 848–863 | Cite as

Hot Spots of Inorganic Nitrogen Availability in an Alpine-Subalpine Ecosystem, Colorado Front Range

  • Anthony Darrouzet-Nardi
  • William. D. Bowman


Inorganic nitrogen (N) availability hot spots have been documented in many ecosystems, but major uncertainties remain about their prevalence, timing, and causes. Using a novel mathematical definition of hot spots, spatially explicit measurements of KCl-extractable inorganic N, 2-week soil incubations in the field, ion-exchange resins deployed for 1 year, and a set of associated biotic and abiotic variables, we investigated inorganic N availability hot spots within a 0.89 km2 alpine-subalpine ecosystem in the Colorado Front Range. Measurements of KCl-extractable NH4 + and NO3 taken on multiple dates showed that hot spots of N availability were present in some but not all parts of the study site and that hot spot location varied over the course of the season. Ion-exchange resins showed that over a 1-year period hot spots were important contributors to resin-available N at the landscape level, with 14% of resin locations accounting for 58% of total resin-extractable inorganic N. The KCl-extractable and resin-available inorganic N measurements showed that although spatial variation in the timing of hot spots (that is, hot moments) spreads the influence of short-term hot spots across the landscape to some extent, spatial variation in inorganic N availability is still important when integrated over 1 year. Resin-available N was poorly correlated with the biotic and abiotic variables that we measured, though we did observe that hot spots of resin-available N were twice as common below tree and shrub canopies than in herbaceous areas. Beyond this relationship with canopy structure, neither KCl-extractable nor resin-available inorganic N hot spots were closely related to plant species identity. Instead, the most effective predictor of KCl-extractable NH4 + was the size of the soil organic matter (SOM) N pool, with nearly all hot spots appearing in soils that had greater than 1.4% SOM N.

Key words

nutrient availability Lorenz curve spatially explicit inequality Niwot Ridge LTER random forest model disproportion 



For funding, we thank NSF DGE 0202758, NSF DEB 0423662, NSF DEB 0808275, the John W. Marr Ecology Fund, and the Department of Ecology and Evolutionary Biology. For helpful suggestions on this manuscript, we thank Alan Townsend, Carol Wessman, Tim Seastedt, and Mark Williams, Michael Weintraub, and Zachary Rinkes. For their help in the field, lab, and/or planning stages of this project, we thank Courtney Meier, John Murgel, Carly Baroch, Brendan Whyte, Anna Lieb, Jaclyn Darrouzet-Nardi, Jeanette Darrouzet-Nardi, Chris Darrouzet-Nardi, Kathy Buehmann, Lisa Gerstenberger, David Knochel, Russ Monson, Stuart Grandy, Courtney Meier, Andy Thomspon, Todd Ackerman, and the numerous volunteers on the July 9th and 30th 2008 field days as well as during the snow sampling effort. We thank Chris Seibold and the Kiowa Lab assistants for help with nutrient analyses. Logistical support was provided the University of Colorado’s Mountain Research Station. Finally, we thank the reviewers, whose careful consideration and suggestions greatly improved this manuscript.

Supplementary material

10021_2011_9450_MOESM1_ESM.pdf (2.4 mb)
Supplementary material 4 (PDF 2,408 kb)


  1. Aber JD, Magill A, Boone R, Melillo JM, Steudler P, Bowden R. 1993. Plant and soil responses to chronic nitrogen additions at the Harvard Forest, Massachusetts. Ecol Appl 3:156–66.CrossRefGoogle Scholar
  2. Armstrong DM, Halfpenny JC, Southwick CH. 2001. Vertebrates. In: Bowman WD, Seastedt TR, Eds. Structure and function of an alpine ecosystem: Niwot Ridge, Colorado. Oxford (NY): Oxford University Press. p 128–56.Google Scholar
  3. Bengtson P, Basiliko N, Prescott CE, Grayston SJ. 2007. Spatial dependency of soil nutrient availability and microbial properties in a mixed forest of Tsuga heterophylla and Pseudotsuga menziesii, in coastal British Columbia, Canada. Soil Biol Biochem 39:2429–35.CrossRefGoogle Scholar
  4. Bogaert N, Salomez J, Vermoesen A, Hofman G, Van Cleemput O, Van Meirvenne M. 2000. Within-field variability of mineral nitrogen in grassland. Biol Fertil Soils 32:186–93.CrossRefGoogle Scholar
  5. Bowman WD, Theodose TA, Schardt JC, Conant RT. 1993. Constraints of nutrient availability on primary production in 2 alpine tundra communities. Ecology 74:2085–97.CrossRefGoogle Scholar
  6. Breiman L. 2001. Random forests. Mach Learn 45:5–32.CrossRefGoogle Scholar
  7. Britto DT, Kronzucker HJ. 2002. NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159:567–84.CrossRefGoogle Scholar
  8. Burns DA. 2003. Atmospheric nitrogen deposition in the Rocky Mountains of Colorado and southern Wyoming—a review and new analysis of past study results. Atmos Environ 37:921–32.CrossRefGoogle Scholar
  9. Callesen I, Borken W, Kalbitz K, Matzner E. 2007. Long-term development of nitrogen fluxes in a coniferous ecosystem: does soil freezing trigger nitrate leaching? J Plant Nutr Soil Sci 170:189–96.CrossRefGoogle Scholar
  10. Cheng X, An S, Chen J, Li B, Liu Y, Liu S. 2007. Spatial relationships among species, above-ground biomass, N, and P in degraded grasslands in Ordos Plateau, northwestern China. J Arid Environ 68:652–67.CrossRefGoogle Scholar
  11. Darrouzet-Nardi A. 2010. Landscape heterogeneity of differently aged soil organic matter constituents at the forest-alpine tundra ecotone, Niwot Ridge, Colorado, U.S.A. Arct Antarct Alp Res 42:179–87.CrossRefGoogle Scholar
  12. Dick DA, Gilliam FS. 2007. Spatial heterogeneity and dependence of soils and herbaceous plant communities in adjacent seasonal wetland and pasture sites. Wetlands 27:951–63.CrossRefGoogle Scholar
  13. Eno CF. 1960. Nitrate production on the field by incubating the soil in polyethylene bags. Soil Sci Soc Proc 24:277–89.CrossRefGoogle Scholar
  14. Ettema CH, Coleman DC, Vellidis G, Lowrance R, Rathbun SL. 1998. Spatiotemporal distributions of bacterivorous nematodes and soil resources in a restored riparian wetland. Ecology 79:2721–34.CrossRefGoogle Scholar
  15. Fenn ME, Baron JS, Allen EB, Rueth HM, Nydick KR, Geiser L, Bowman WD, Sickman JO, Meixner T, Johnson DW, Neitlich P. 2003. Ecological effects of nitrogen deposition in the western United States. Bioscience 53:404–20.CrossRefGoogle Scholar
  16. Fraterrigo JM, Turner MG, Pearson SM, Dixon P. 2005. Effects of past land use on spatial heterogeneity of soil nutrients in southern Appalachian forests. Ecol Monogr 75:215–30.CrossRefGoogle Scholar
  17. Gallardo A. 2003. Effect of tree canopy on the spatial distribution of soil nutrients in a Mediterranean Dehesa. Pedobiologia 47:117–25.CrossRefGoogle Scholar
  18. Gallardo A, Covelo F. 2005. Spatial pattern and scale of leaf N and P concentration in a Quercus robur population. Plant Soil 273:269–77.CrossRefGoogle Scholar
  19. Gallardo A, Parama R, Covelo F. 2005. Soil ammonium vs. nitrate spatial pattern in six plant communities: simulated effect on plant populations. Plant Soil 277:207–19.CrossRefGoogle Scholar
  20. Gallardo A, Parama R, Covelo F. 2006. Differences between soil ammonium and nitrate spatial pattern in six plant communities. Simulated effect on plant populations. Plant Soil 279:333–46.CrossRefGoogle Scholar
  21. Gastwirth JL. 1972. The estimation of the Lorenz curve and Gini index. Rev Econ Stat 54:306–16.CrossRefGoogle Scholar
  22. Ghidey F, Alberts EE. 1999. Temporal and spatial patterns of nitrate in a claypan soil. J Environ Qual 28:584–94.CrossRefGoogle Scholar
  23. Gonzalez OJ, Zak DR. 1994. Geostatistical analysis of soil properties in a secondary tropical dry forest, St-Lucia, West-Indies. Plant Soil 163:45–54.Google Scholar
  24. Goovaerts P, Chiang CN. 1993. Temporal persistence of spatial patterns for mineralizable nitrogen and selected soil properties. Soil Sci Soc Am J 57:372–81.CrossRefGoogle Scholar
  25. Groffman PM, Butterbach-Bahl K, Fulweiler RW, Gold AJ, Morse JL, Stander EK, Tague C, Tonitto C, Vidon P. 2009. Challenges to incorporating spatially and temporally explicit phenomena (hotspots and hot moments) in denitrification models. Biogeochemistry 93:49–77.CrossRefGoogle Scholar
  26. Grubbs FE. 1950. Sample criteria for testing outlying observations. Ann Math Stat 21:27–58.CrossRefGoogle Scholar
  27. Hastie T, Tibshirani R, Friedman JH. 2001. The elements of statistical learning: data mining, inference, and prediction: with 200 full-color illustrations. New York: Springer.Google Scholar
  28. Hoaglin DC, Mosteller F, Tukey JW. 1983. Understanding robust and exploratory data analysis. New York: Wiley.Google Scholar
  29. Jackson RB, Caldwell MM. 1993. Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81:683–92.CrossRefGoogle Scholar
  30. John R, Dalling JW, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M, Foster RB. 2007. Soil nutrients influence spatial distributions of tropical tree species. Proc Natl Acad Sci USA 104:864–9.PubMedCrossRefGoogle Scholar
  31. Johnson DW, Glass DW, Murphy JD, Stein CM, Miller WW. 2010. Nutrient hot spots in some Sierra Nevada forest soils. Biogeochemistry 101:93–103.CrossRefGoogle Scholar
  32. Kristensen HL, Gundersen P, Callesen I, Reinds GJ. 2004. Throughfall nitrogen deposition has different impacts on soil solution nitrate concentration in European coniferous and deciduous forests. Ecosystems 7:180–92.CrossRefGoogle Scholar
  33. Lajtha K. 1988. The use of ion-exchange resin bags for measuring nutrient availability in an arid ecosystem. Plant Soil 105:105–11.CrossRefGoogle Scholar
  34. Liaw A, Wiener M. 2002. Classification and regression by randomForest. R News 2:18–22.Google Scholar
  35. Liptzin D, Seastedt TR. 2009. Patterns of snow, deposition, and soil nutrients at multiple spatial scales at a Rocky Mountain tree line ecotone. J Geophys Res Biogeo 114. doi: 10.1029/2009JG000941.
  36. Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P. 2004. Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. For Ecol Manag 196:7–28.CrossRefGoogle Scholar
  37. McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G. 2003. Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–12.CrossRefGoogle Scholar
  38. Meier CL, Bowman WD. 2008. Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proc Natl Acad Sci USA 105:19780–5.PubMedCrossRefGoogle Scholar
  39. Mellert KH, Gensior A, Gottlein A, Kolling C, Rucker G. 2008. Variation in soil nitrate concentrations in two n-saturated norway spruce forests (Picea abies (L.) karst.) in southern Bavaria. Water Air Soil Pollut 187:203–17.CrossRefGoogle Scholar
  40. Moorhead DL, Sinsabaugh RL. 2006. A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–74.CrossRefGoogle Scholar
  41. Okin GS, Mladenov N, Wang L, Cassel D, Caylor KK, Ringrose S, Macko SA. 2008. Spatial patterns of soil nutrients in two southern African savannas. J Geophys Res Biogeo 113. doi: 10.1029/2007JG000584.
  42. Pennock DJ, Vankessel C, Farrell RE, Sutherland RA. 1992. Landscape-scale variations in denitrification. Soil Sci Soc Am J 56:770–6.CrossRefGoogle Scholar
  43. R Development Core Team. 2007. R 2.6.0: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
  44. Rivero RG, Grunwald S, Osborne TZ, Reddy KR, Newman S. 2007. Characterization of the spatial distribution of soil properties in water conservation area 2A, Everglades, Florida. Soil Sci 172:149–66.CrossRefGoogle Scholar
  45. Robertson GP, Huston MA, Evans FC, Tiedje JM. 1988. Spatial variability in a successional plant community—patterns of nitrogen availability. Ecology 69:1517–24.CrossRefGoogle Scholar
  46. Robertson GP, Klingensmith KM, Klug MJ, Paul EA, Crum JR, Ellis BG. 1997. Soil resources, microbial activity, and primary production across an agricultural ecosystem. Ecol Appl 7:158–70.CrossRefGoogle Scholar
  47. Rodionov A, Flessa H, Grabe M, Kazansky OA, Shibistova O, Guggenberger G. 2007. Organic carbon and total nitrogen variability in permafrost-affected soils in a forest tundra ecotone. Eur J Soil Sci 58:1260–72.CrossRefGoogle Scholar
  48. Schimel JP, Bennett J. 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602.CrossRefGoogle Scholar
  49. Seastedt TR, Bowman WD, Caine TN, McKnight D, Townsend A, Williams MW. 2004. The landscape continuum: a model for high-elevation ecosystems. Bioscience 54:111–21.CrossRefGoogle Scholar
  50. Sibbeson EA. 1977. Simple ion-exchange resin procedure for extracting plant available elements from soil. Plant Soil 46:665–9.CrossRefGoogle Scholar
  51. Steltzer H, Bowman WD. 1998. Differential influence of plant species on soil nitrogen transformations within moist meadow Alpine tundra. Ecosystems 1:464–74.CrossRefGoogle Scholar
  52. Stenger R, Priesack E, Beese F. 1998. Distribution of inorganic nitrogen in agricultural soils at different dates and scales. Nutr Cycl Agroecosyst 50:291–7.CrossRefGoogle Scholar
  53. Stenger R, Priesack E, Beese F. 2002. Spatial variation of nitrate-N and related soil properties at the plot-scale. Geoderma 105:259–75.CrossRefGoogle Scholar
  54. Strayer DL. 2005. Challenges in understanding the functions of ecological heterogeneity. In: Lovett GM, Jones CG, Turner MG, Weathers KC, Eds. Ecosystem function in heterogeneous landscapes. New York: Springer. p 411–25.CrossRefGoogle Scholar
  55. Townsend AR, Asner GP, Cleveland CC. 2008. The biogeochemical heterogeneity of tropical forests. Trends Ecol Evol 23:424–31.PubMedCrossRefGoogle Scholar
  56. van der Loo MPJ. 2010. Distribution based outlier detection in univariate data. The Hague: Statistics Netherlands. pp 1–14.Google Scholar
  57. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea—how can it occur. Biogeochemistry 13:87–115.CrossRefGoogle Scholar
  58. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50.Google Scholar
  59. Vitousek P, Chadwick O, Matson P, Allison S, Derry L, Kettley L, Luers A, Mecking E, Monastra V, Porder S. 2003. Erosion and the rejuvenation of weathering-derived nutrient supply in an old tropical landscape. Ecosystems 6:762–72.CrossRefGoogle Scholar
  60. Wang LX, Mou PP, Huang JH, Wang J. 2007. Spatial heterogeneity of soil nitrogen in a subtropical forest in China. Plant Soil 295:137–50.CrossRefGoogle Scholar
  61. Weintraub MN, Schimel JP. 2005. The seasonal dynamics of amino acids and other nutrients in Alaskan Arctic tundra soils. Biogeochemistry 73:359–80.CrossRefGoogle Scholar
  62. Yanai J, Lee CK, Umeda M, Kosaki T. 2000. Spatial variability of soil chemical properties in a paddy field. Soil Sci Plant Nutr 46:473–82.Google Scholar
  63. Yavitt JB, Wright SJ. 1996. Temporal patterns of soil nutrients in a Panamanian moist forest revealed by ion-exchange resin and experimental irrigation. Plant Soil 183:117–29.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Anthony Darrouzet-Nardi
    • 1
    • 2
    • 3
  • William. D. Bowman
    • 1
    • 3
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of Colorado at BoulderBoulderUSA
  2. 2.Department of Environmental SciencesUniversity of ToledoToledoUSA
  3. 3.Mountain Research StationInstitute of Arctic and Alpine Research, University of ColoradoBoulderUSA

Personalised recommendations