, Volume 19, Issue 1, pp 50–61 | Cite as

Disturbance Decouples Biogeochemical Cycles Across Forests of the Southeastern US

  • Ashley D. KeiserEmail author
  • Jennifer D. Knoepp
  • Mark A. Bradford


Biogeochemical cycles are inherently linked through the stoichiometric demands of the organisms that cycle the elements. Landscape disturbance can alter element availability and thus the rates of biogeochemical cycling. Nitrification is a fundamental biogeochemical process positively related to plant productivity and nitrogen loss from soils to aquatic systems, and the rate of nitrification is sensitive to both carbon and nitrogen availability. Yet how these controls influence nitrification rates at the landscape scale is not fully elucidated. We, therefore, sampled ten watersheds with different disturbance histories in the southern Appalachian Mountains to examine effects on potential net nitrification rates. Using linear mixed model selection (AIC), we narrowed a broad suite of putative explanatory variables into a set of models that best explained landscape patterns in potential net nitrification. Forest disturbance history determined whether nitrification and nitrogen mineralization were correlated, with the effect apparently mediated by microbially available carbon. Undisturbed forests had higher available carbon, which uncoupled potential net nitrification from potential net nitrogen mineralization. In contrast, disturbed watersheds had lower available carbon, and nitrification rates were strongly correlated to those of nitrogen mineralization. These data suggest that a history of disturbance at the landscape scale reduces soil carbon availability, which increases ammonium availability to nitrifiers at the micro-scale. Landscape-level soil carbon availability then appears to determine the coupling of autotrophic (nitrification) and heterotrophic (nitrogen mineralization) biogeochemical processes, and hence the relationship between carbon and nitrogen cycling in soils.


autotroph carbon cycle competition disturbance heterotroph net nitrification nitrogen cycle nitrogen mineralization scale-dependence watershed ecology 



Funding was through a co-operative agreement from the USDA Forest Service, the Coweeta Hydrologic Laboratory, and from the National Science Foundation to the Coweeta LTER. We thank David Keiser for field assistance. We also thank Stephen Hart and two anonymous reviewers for their improvements to this manuscript.

Supplementary material

10021_2015_9917_MOESM1_ESM.docx (55 kb)
Supplementary material 1 (DOCX 55 kb)


  1. Allen SE. 1989. Chemical analysis of ecological materials. Oxford: Blackwell Scientific.Google Scholar
  2. Bernhardt ES, Hall JRO, Likens GE. 2002. Whole-system estimates of nitrification and nitrate uptake in streams of the Hubbard Brook Experimental Forest. Ecosystems 5:419–30.CrossRefGoogle Scholar
  3. Bernhardt ES, Likens GE. 2002. Dissolved organic carbon enrichment alters nitrogen dynamics in a forest stream. Ecology 83:1689–700.CrossRefGoogle Scholar
  4. Bonkowski M. 2004. Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist 162:617–31.CrossRefGoogle Scholar
  5. Booth MS, Stark JM, Hart SC. 2006. Soil-mixing effects on inorganic nitrogen production and consumption in forest and shrubland soils. Plant Soil 289:5–15.CrossRefGoogle Scholar
  6. Booth MS, Stark JM, Rastetter E. 2005. Controls on nitrogen cycling in terrestrial ecosystems: A synthetic analysis of literature data. Ecol Monogr 75:139–57.CrossRefGoogle Scholar
  7. Bormann FH, Likens GE. 1979. Catastrophic disturbance and the steady-state in northern hardwood forests. Am Scientist 67:660–9.Google Scholar
  8. Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, Reynolds JF, Treseder KK, Wallenstein MD. 2008a. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–27.CrossRefPubMedGoogle Scholar
  9. Bradford MA, Fierer N, Reynolds JF. 2008b. Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils. Funct Ecol 22:964–74.CrossRefGoogle Scholar
  10. Bradford MA, Warren RJII, Baldrian P, Crowther TW, Maynard DS, Oldfield EE, Wieder WR, Wood SA, King JR. 2014. Climate fails to predict wood decomposition at regional scales. Nat Clim Change 4:625–30.CrossRefGoogle Scholar
  11. Clarholm M. 1985. Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–7.CrossRefGoogle Scholar
  12. Cottingham KL, Lennon JT, Brown BL. 2005. Knowing when to draw the line: designing more informative ecological experiments. Front Ecol Environ 3:145–52.CrossRefGoogle Scholar
  13. Davey ME, O’Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–67.PubMedCentralCrossRefPubMedGoogle Scholar
  14. Dechesne A, Pallud C, Grundmann GL. 2007. Spatial distribution of bacteria at the microscale in soil. In: Franklin RB, Mills AL, Eds. The spatial distribution of microbes in the environment. Berlin: Springer. p 87–107.CrossRefGoogle Scholar
  15. Dijkstra P, LaViolette CM, Coyle JS, Doucett RR, Schwartz E, Hart SC, Hungate BA. 2008. 15 N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecol Lett 11:389–97.CrossRefPubMedGoogle Scholar
  16. Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJP, Oren R, Palmroth S, Phillips RP, Pippen JS, Pritchard SG, Treseder KK, Schlesinger WH, DeLucia EH, Finzi AC. 2011. Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–57.CrossRefPubMedGoogle Scholar
  17. Fierer N, Craine JM, McLauchlan K, Schimel JP. 2005. Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–6.CrossRefGoogle Scholar
  18. Fierer N, Schimel JP. 2002. Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem 34:777–87.CrossRefGoogle Scholar
  19. Fierer N, Schimel JP. 2003. A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sc Soc Am J 67:798–805.CrossRefGoogle Scholar
  20. Finzi AC, Austin AT, Cleland EE, Frey SD, Houlton BZ, Wallenstein MD. 2011. Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Front Ecol Environ 9:61–7.CrossRefGoogle Scholar
  21. Flinn KM, Vellend M, Marks PL. 2005. Environmental causes and consequences of forest clearance and agricultural abandonment in central New York, USA. J Biogeogr 32:439–52.CrossRefGoogle Scholar
  22. 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
  23. Goodale CL, Aber JD. 2001. The long-term effects of land-use history on nitrogen cycling in northern hardwood forests. Ecol Appl 11:253–67.CrossRefGoogle Scholar
  24. Grundmann GL, Dechesne A, Bartoli F, Flandrois JP, Chasse JL, Kizungu R. 2001. Spatial modeling of nitrifier microhabitats in soil. Soil Sci Soc Am J 65:1709–16.CrossRefGoogle Scholar
  25. Guo LB, Gifford RM. 2002. Soil carbon stocks and land use change: a meta analysis. Global Change Biol 8:345–60.CrossRefGoogle Scholar
  26. Hart SC, Nason GE, Myrold DD, Perry DA. 1994. Dynamics of gross nitrogen transformations in an old-growth forest—the carbon connection. Ecology 75:880–91.CrossRefGoogle Scholar
  27. Kaye JP, Hart SC. 1997. Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–43.CrossRefPubMedGoogle Scholar
  28. Knoepp JD, Coleman DC, Crossley DA, Clark JS. 2000. Biological indices of soil quality: an ecosystem case study of their use. For Ecol Manag 138:357–68.CrossRefGoogle Scholar
  29. Knoepp JD, Swank WT. 1995. Comparison of available soil nitrogen assays in control and burned forested sites. Soil Sci Soc Am J 59:1750–4.CrossRefGoogle Scholar
  30. Knoepp JD, Swank WT. 1997. Forest management effects on surface soil carbon and nitrogen. Soil Sci Soc Am J 61:928–35.CrossRefGoogle Scholar
  31. Knoepp JD, Swank WT, Haines BL. 2014. Long- and short-term changes in nutrient availability following commercial sawlog harvest via cable logging. In: Swank WT, Webster JR, Eds. Long-term response of a forest watershed ecosystem: clearcutting in the southern Appalachians. London: Oxford University Press. Google Scholar
  32. Kramer TD, Warren RJ, Tang YY, Bradford MA. 2012. Grass invasions across a regional gradient are associated with declines in belowground carbon pools. Ecosystems 15:1271–82.CrossRefGoogle Scholar
  33. Lavoie M, Bradley RL. 2003. Short-term increases in relative nitrification rates due to trenching in forest floor and mineral soil horizons of different forest types. Plant Soil 252:367–84.CrossRefGoogle Scholar
  34. Liao CZ, Luo YQ, Fang CM, Li B. 2010. Ecosystem carbon stock influenced by plantation practice: implications for planting forests as a measure of climate change mitigation. Plos One 5(5):e10867.PubMedCentralCrossRefPubMedGoogle Scholar
  35. Lovett GM, Rueth H. 1999. Soil nitrogen transformations in beech and maple stands along a nitrogen deposition gradient. Ecol Appl 9:1330–44.CrossRefGoogle Scholar
  36. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–9.CrossRefPubMedGoogle Scholar
  37. McGill WB, Cole CV. 1981. Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–86.CrossRefGoogle Scholar
  38. McGinty DT. 1976. Comparative root and soil dynamics on a white pine watershed and in the hardwood forest in the Coweeta basin. Athens, GA: Institute of Ecology, University of Georgia. p 110.Google Scholar
  39. Murty D, Kirschbaum MUF, McMurtrie RE, McGilvray H. 2002. Does conversion of forest to agricultural land change soil carbon and nitrogen? a review of the literature. Global Change Biol 8:105–23.CrossRefGoogle Scholar
  40. Neff JC, Townsend AR, Gleixner G, Lehman SJ, Turnbull J, Bowman WD. 2002. Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–17.CrossRefPubMedGoogle Scholar
  41. Nuckolls A, Wurzburger N, Ford C, Hendrick R, Vose J, Kloeppel B. 2009. Hemlock declines rapidly with hemlock woolly adelgid infestation: Impacts on the carbon cycle of southern Appalachian forests. Ecosystems 12:179–90.CrossRefGoogle Scholar
  42. Nunan N, Wu KJ, Young IM, Crawford JW, Ritz K. 2003. Spatial distribution of bacterial communities and their relationships with the micro-architecture of soil. Fems Microbiol Ecol 44:203–15.CrossRefPubMedGoogle Scholar
  43. Parker SS, Schimel JP. 2011. Soil nitrogen availability and transformations differ between the summer and the growing season in a California grassland. Appl Soil Ecol 48:185–92.CrossRefGoogle Scholar
  44. Perala DA, Alban DH. 1982. Rates of forest floor decomposition and nutrient turnover in aspen, pine and spruce stands on two different soils. Res. Pap. NC-227. St. Paul, MN: U.S. Department of Agriculture, Forest Service, North Central Forest Experimental Station, 5.Google Scholar
  45. Phillips RP, Finzi AC, Bernhardt ES. 2011. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–94.CrossRefPubMedGoogle Scholar
  46. Prosser JI, Nicol GW. 2012. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–31.CrossRefPubMedGoogle Scholar
  47. Qian JH, Doran JW, Walters DT. 1997. Maize plant contributions to root zone available carbon and microbial transformations of nitrogen. Soil Biol Biochem 29:1451–62.CrossRefGoogle Scholar
  48. R Development Core Team 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  49. Robertson GP, Wedin D, Groffman PM, Blair JM, Holland EA, Nadelhoffer KJ, Harris D. 1999. Soil carbon and nitrogen availability: nitrogen mineralization, nitrification, and soil respiration potentials. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P, Eds. Standard soil methods for long-term ecological research. New York: Oxford University Press. p 258–71.Google Scholar
  50. Schimel JP, Bennett J. 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602.CrossRefGoogle Scholar
  51. Schimel JP, Weintraub MN. 2003. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563.CrossRefGoogle Scholar
  52. Schlesinger W. 1986. Changes in soil carbon storage and associated properties with disturbance and recovery. In: Trabalka J, Reichle D, Eds. The changing carbon cycle. New York: Springer. p 194–220.CrossRefGoogle Scholar
  53. Schlesinger WH, Cole JJ, Finzi AC, Holland EA. 2011. Introduction to coupled biogeochemical cycles. Front Ecol Environ 9:5–8.CrossRefGoogle Scholar
  54. Silva RG, Jorgensen EE, Holub SM, Gonsoulin ME. 2005. Relationships between culturable soil microbial populations and gross nitrogen transformation processes in a clay loam soil across ecosystems. Nutr Cycl Agroecosyst 71:259–70.CrossRefGoogle Scholar
  55. Stark JM, Firestone MK. 1995. Mechanisms for soil-moisture effects on activity of nitrifying bacteria. Appl Environ Microbiol 61:218–21.PubMedCentralPubMedGoogle Scholar
  56. Stark JM, Hart SC. 1997. High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature 385:61–4.CrossRefGoogle Scholar
  57. Strauss EA, Lamberti AG. 2000. Regulation of nitrification in aquatic sediments by organic carbon. Waco: American Society of Limnology and Oceanography.Google Scholar
  58. Swank WT, Knoepp JD, Vose JM, Laseter S, Webster JR. 2014. Response and recovery of water yield and timing, stream sediment, abiotic parameters, and stream chemistry following logging. In: Swank WT, Webster JR, Eds. Long-term response of a forest watershed ecosystem: clearcutting in the southern Appalachians. London: Oxford University Press. CrossRefGoogle Scholar
  59. van der Heijden MGA, Bardgett RD, van Straalen NM. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310.CrossRefPubMedGoogle Scholar
  60. Verhagen FJ, Duyts H, Laanbroek HJ. 1992. Competition for ammonium between nitrifying and heterotrophic bacteria in continuously percolated soil columns. Appl Environ Microbiol 58:3303–11.PubMedCentralPubMedGoogle Scholar
  61. Verhagen FJ, Laanbroek HJ. 1991. Competition for ammonium between nitrifying and heterotrophic bacteria in dual energy-limited chemostats. Appl Environ Microbiol 57:3255–63.PubMedCentralPubMedGoogle Scholar
  62. Viviroli D, Durr HH, Messerli B, Meybeck M, Weingartner R. 2007. Mountains of the world, water towers for humanity: typology, mapping, and global significance. Water Resour Res 43(7):W07447.CrossRefGoogle Scholar
  63. Warren RJ, Bradford MA. 2011. The shape of things to come: woodland herb niche contraction begins during recruitment in mesic forest microhabitat. Proc R Soc B 278:1390–8.PubMedCentralCrossRefPubMedGoogle Scholar
  64. West AW, Sparling GP. 1986. Modifications to the substrate-induced respiration method to permit measurement of microbial biomass in soils of differing water contents. J Microbiol Methods 5:177–89.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Ashley D. Keiser
    • 1
    • 2
    Email author
  • Jennifer D. Knoepp
    • 3
  • Mark A. Bradford
    • 1
  1. 1.School of Forestry and Environmental StudiesYale UniversityNew HavenUSA
  2. 2.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA
  3. 3.USDA Forest Service Southern Research StationCoweeta Hydrologic LaboratoryOttoUSA

Personalised recommendations