, Volume 141, Issue 3, pp 523–539 | Cite as

Nitrogen oligotrophication in northern hardwood forests

  • Peter M. GroffmanEmail author
  • Charles T. Driscoll
  • Jorge Durán
  • John L. Campbell
  • Lynn M. Christenson
  • Timothy J. Fahey
  • Melany C. Fisk
  • Colin Fuss
  • Gene E. Likens
  • Gary Lovett
  • Lindsey Rustad
  • Pamela H. Templer


While much research over the past 30 years has focused on the deleterious effects of excess N on forests and associated aquatic ecosystems, recent declines in atmospheric N deposition and unexplained declines in N export from these ecosystems have raised new concerns about N oligotrophication, limitations of forest productivity, and the capacity for forests to respond dynamically to disturbance and environmental change. Here we show multiple data streams from long-term ecological research at the Hubbard Brook Experimental Forest in New Hampshire, USA suggesting that N oligotrophication in forest soils is driven by increased carbon flow from the atmosphere through soils that stimulates microbial immobilization of N and decreases available N for plants. Decreased available N in soils can result in increased N resorption by trees, which reduces litterfall N input to soils, further limiting available N supply and leading to further declines in soil N availability. Moreover, N oligotrophication has been likely exacerbated by changes in climate that increase the length of the growing season and decrease production of available N by mineralization during both winter and spring. These results suggest a need to re-evaluate the nature and extent of N cycling in temperate forests and assess how changing conditions will influence forest ecosystem response to multiple, dynamic stresses of global environmental change.


Climate change Carbon Dissolved organic carbon Hubbard Brook Experimental Forest Nitrogen 



This research was supported by grants from the U.S. National Science Foundation programs in Ecosystem Studies, Long-Term Ecological Research and Long-Term Ecological Research in Environmental Biology and from the Andrew W. Mellon Foundation. J.D. was supported by a Fulbright fellowship of the Spanish Ministry of Education and by a FCT Research Fellowship of the Portuguese Ministry of Education and Science (SFRH/BDP/87966/2012).


  1. Aber JD, Driscoll CT (1997) Effects of land use, climate variation, and N deposition on N cycling and C storage in northern hardwood forests. Global Biogeochem Cycles 11(4):639–648Google Scholar
  2. Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. Bioscience 39(6):378–386Google Scholar
  3. Aber JD, Goodale CL, Ollinger SV, Smith ML, Magill AH, Martin ME, Hallett RA, Stoddard JL (2003) Is nitrogen deposition altering the nitrogen status of northeastern forests? Bioscience 53(4):375–389Google Scholar
  4. Andresen LC, Michelsen A (2005) Off-season uptake of nitrogen in temperate heath vegetation. Oecologia 144(4):585–597Google Scholar
  5. Battles JJ, Fahey TJ, Driscoll CT Jr, Blum JD, Johnson CE (2014) Restoring soil calcium reverses forest decline. Environ. Sci. Technol. Lett. 1(1):15–19Google Scholar
  6. Battye W, Aneja VP, Schlesinger WH (2017) Is nitrogen the next carbon? Earth’s Future 5(9):894–904Google Scholar
  7. Bernal S, Hedin LO, Likens GE, Gerber S, Buso DC (2012) Complex response of the forest nitrogen cycle to climate change. Proc Natl Acad Sci USA 109(9):3406–3411Google Scholar
  8. Bernhardt ES, Likens GE, Hall RO, Buso DC, Fisher SG, Burton TM, Meyer JL, McDowell WH, Mayer MS, Bowden WB, Findlay SEG, Macneale KH, Stelzer RS, Lowe WH (2005) Can’t see the forest for the stream? In-stream processing and terrestrial nitrogen exports. Bioscience 55(3):219–230Google Scholar
  9. Bohlen PJ, Groffman PM, Driscoll CT, Fahey TJ, Siccama TG (2001) Plant-soil-microbial interactions in a northern hardwood forest. Ecology 82(4):965–978Google Scholar
  10. Bormann FH, Likens GE (1979) Pattern and process in a forested ecosystem. Springer, New YorkGoogle Scholar
  11. Bowden RD, Melillo JM, Steudler PA, Aber JD (1991) Effects of nitrogen additions on annual nitrous-oxide fluxes from temperate forest soils in the northeastern United States. J Geophys Res Atmos 96(D5):9321–9328Google Scholar
  12. Brooks PD, Grogan P, Templer PH, Groffman PM, Oquist MG, Schimel J (2011) Carbon and nitrogen cycling in snow-covered environments. Geogr Compass 5(9):682–699Google Scholar
  13. Campbell JL, Mitchell MJ, Groffman PM, Christenson LM, Hardy JP (2005) Winter in northeastern North America: a critical period for ecological processes. Front Ecol Environ 3(6):314–322Google Scholar
  14. Campbell JL, Driscoll CT, Eagar C, Likens GE, Siccama TG, Johnson CE, Fahey TJ, Hamburg SP, Holmes RT, Bailey AS, Buso DC (2007a) Long-term trends from ecosystem research at the Hubbard Brook Experimental Forest. General Technical Report NRS-17. U.S. Department of Agriculture, Forest Service, Northern Research Station Newtown Square, PAGoogle Scholar
  15. Campbell JL, Mitchell MJ, Mayer B, Groffman PM, Christenson LM (2007b) Mobility of nitrogen-15-labeled nitrate and sulfur-34-labeled sulfate during snowmelt. Soil Sci Soc Am J 71(6):1934–1944Google Scholar
  16. Campbell JL, Socci AM, Templer PH (2014) Increased nitrogen leaching following soil freezing is due to decreased root uptake in a northern hardwood forest. Glob Change Biol 20(8):2663–2673Google Scholar
  17. Chapin FS, Schulze E, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21(1):423–447Google Scholar
  18. Cho Y, Driscoll C, Johnson C, Blum J, Fahey T (2012) Watershed-level responses to calcium silicate treatment in a northern hardwood forest. Ecosystems 15(3):416–434Google Scholar
  19. Cleavitt NL, Fahey TJ, Groffman PM, Hardy JP, Henry KS, Driscoll CT (2008) Effects of soil freezing on fine roots in a northern hardwood forest. Can J For Res 38(1):82–91Google Scholar
  20. Comerford D, Schaberg P, Templer P, Socci A, Campbell J, Wallin K (2013) Influence of experimental snow removal on root and canopy physiology of sugar maple trees in a northern hardwood forest. Oecologia 171:261–269Google Scholar
  21. Davidson EA, David MB, Galloway JN, Goodale CL, Haeuber R, Harrison JA, Howarth RW, Jaynes DB, Lowrance RR, Nolan BT, Peel JL, Pinder RW, Porter E, Snyder CS, Townsend AR, Ward MH (2012) Excess nitrogen in the U.S. environment: trends, risks, and solutions. Issues Ecol 15:1–16Google Scholar
  22. Dawson JJC, Malcolm IA, Middlemas SJ, Tetzlaff D, Soulsby C (2009) Is the composition of dissolved organic carbon changing in upland acidic streams? Environ Sci Technol 43(20):7748–7753Google Scholar
  23. Dittman JA, Driscoll CT, Groffman PM, Fahey TJ (2007) Dynamics of nitrogen and dissolved organic carbon at the Hubbard Brook Experimental Forest. Ecology 88(5):1153–1166Google Scholar
  24. 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(4):349–357Google Scholar
  25. Driscoll CT, Lawrence GB, Bulger AJ, Butler TJ, Cronan CS, Eagar C, Lambert KF, Likens GE, Stoddard JL, Weathers KC (2001) Acidic deposition in the northeastern United States: sources and inputs, ecosystem effects, and management strategies. Bioscience 51(3):180–198Google Scholar
  26. Driscoll CT, Driscoll KM, Roy KM, Dukett J (2007) Changes in the chemistry of lakes in the Adirondack region of New York following declines in acidic deposition. Appl Geochem 22:1181–1188Google Scholar
  27. Driscoll CT, Driscoll KM, Fakhraei H, Civerolo K (2016) Long-term temporal trends and spatial patterns in the acid-base chemistry of lakes in the Adirondack region of New York in response to decreases in acidic deposition. Atmos Environ 146:5–14Google Scholar
  28. Durán J, Morse JL, Groffman PM, Campbell JL, Christenson LM, Driscoll CT, Fahey TJ, Fisk MC, Mitchell MJ, Templer PH (2014) Winter climate change affects growing-season soil microbial biomass and activity in northern hardwood forests. Glob Change Biol 20(11):3568–3577Google Scholar
  29. Durán J, Morse JL, Groffman PM, Campbell JL, Christenson LM, Driscoll CT, Fahey TJ, Fisk MC, Likens GE, Melillo JM, Mitchell MJ, Templer PH, Vadeboncoeur MA (2016) Climate change decreases nitrogen pools and mineralization rates in northern hardwood forests. Ecosphere 7(3):e01251Google Scholar
  30. Elmore AJ, Nelson DM, Craine JM (2016) Earlier springs are causing reduced nitrogen availability in North American eastern deciduous forests. Nat Plants 2:16133Google Scholar
  31. Eshleman KN, Sabo RD, Kline KM (2013) Surface water quality is improving due to declining atmospheric N deposition. Environ Sci Technol 47(21):12193–12200Google Scholar
  32. Fahey TJ, Battles JJ, Wilson GF (1998) Responses of early successional northern hardwood forests to changes in nutrient availability. Ecol Monogr 68(2):183–212Google Scholar
  33. Fahey TJ, Heinz AK, Battles JJ, Fisk MC, Driscoll CT, Blum JD, Johnson CE (2016) Fine root biomass declined in response to restoration of soil calcium in a northern hardwood forest. Can J For Res 46(5):738–744Google Scholar
  34. Fakhraei H, Driscoll CT (2015) Proton and aluminum binding properties of organic acids in surface waters of the northeastern U.S. Environ Sci Technol 49(5):2939–2947Google Scholar
  35. Fiorentino I, Fahey TJ, Groffman PM, Driscoll CT, Eagar C, Siccama TG (2003) Initial responses of phosphorus biogeochemistry to calcium addition in a northern hardwood forest ecosystem. Can J For Res 33(10):1864–1873Google Scholar
  36. Fitzhugh RD, Driscoll CT, Groffman PM, Tierney GL, Fahey TJ, Hardy JP (2001) Effects of soil freezing disturbance on soil solution nitrogen, phosphorus, and carbon chemistry in a northern hardwood ecosystem. Biogeochemistry 56(2):215–238Google Scholar
  37. Fuss CB, Driscoll CT, Campbell JL (2015) Recovery from chronic and snowmelt acidification: long-term trends in stream and soil water chemistry at the Hubbard Brook Experimental Forest, New Hampshire, USA. J Geophys Res Biogeosci 120(11):2360–2374Google Scholar
  38. Fuss CB, Driscoll CT, Green MB, Groffman PM (2016a) Hydrologic flowpaths during snowmelt in forested headwater catchments under differing winter climatic and soil frost regimes. Hydrol Process 30(24):4617–4632Google Scholar
  39. Fuss CB, Driscoll CT, Groffman PM, Campbell JL, Christenson LM, Fahey TJ, Fisk MC, Mitchell MJ, Templer PH, Durán J, Morse JL (2016b) Nitrate and dissolved organic carbon mobilization in response to soil freezing variability. Biogeochemistry 131(1):35–47Google Scholar
  40. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320(5878):889–892Google Scholar
  41. Gold AJ, Groffman PM, Addy K, Kellogg DQ, Stolt M, Rosenblatt AE (2001) Landscape attributes as controls on ground water nitrate removal capacity of riparian zones. J Am Water Resour Assoc 37(6):1457–1464Google Scholar
  42. Goodale CL, Aber JD, Vitousek PM (2003) An unexpected nitrate decline in New Hampshire streams. Ecosystems 6(1):75–86Google Scholar
  43. Goodale CL, Aber JD, Vitousek PM, McDowell WH (2005) Long-term decreases in stream nitrate: successional causes unlikely; possible links to DOC? Ecosystems 8(3):334–337Google Scholar
  44. Gosz JR, Likens GE, Bormann FH (1973) Nutrient release from decomposing leaf and branch litter in the Hubbard Brook Forest, New Hampshire. Ecol Monogr 43(2):173–191Google Scholar
  45. Groffman PM, Fisk MC (2011) Calcium constrains plant control over forest ecosystem nitrogen cycling. Ecology 92:2035–2042Google Scholar
  46. Groffman PM, Zak DR, Christensen S, Mosier A, Tiedje JM (1993) Early spring nitrogen dynamics in a temperate forest landscape. Ecology 74(5):1579–1585Google Scholar
  47. Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL (2001) Effects of mild winter freezing on soil nitrogen and carbon dynamics in a northern hardwood forest. Biogeochemistry 56(2):191–213Google Scholar
  48. Groffman PM, Fisk MC, Driscoll CT, Likens GE, Fahey TJ, Eagar C, Pardo LH (2006a) Calcium additions and microbial nitrogen cycle processes in a northern hardwood forest. Ecosystems 9(8):1289–1305Google Scholar
  49. Groffman PM, Hardy JP, Driscoll CT, Fahey TJ (2006b) Snow depth, soil freezing, and fluxes of carbon dioxide, nitrous oxide and methane in a northern hardwood forest. Glob Change Biol 12(9):1748–1760Google Scholar
  50. Groffman PM, Hardy JP, Fisk MC, Fahey JT, Driscoll CT (2009) Climate variation and soil carbon and nitrogen cycling processes in a northern hardwood forest. Ecosystems 12:927–943Google Scholar
  51. Groffman P, Hardy J, Fashu-Kanu S, Driscoll C, Cleavitt N, Fahey T, Fisk M (2010) Snow depth, soil freezing and nitrogen cycling in a northern hardwood forest landscape. Biogeochemistry 102(1):223–238Google Scholar
  52. Groffman PM, Rustad LE, Templer PH, Campbell JL, Christenson LM, Lany NK, Socci AM, Vadeboncouer MA, Schaberg PG, Wilson GF, Driscoll CT, Fahey TJ, Fisk MC, Goodale CL, Green MB, Hamburg SP, Johnson CE, Mitchell MJ, Morse JL, Pardo LH, Rodenhouse NL (2012) Long-term integrated studies show that climate change effects are manifest in complex and surprising ways in the northern hardwood forest. Bioscience 62:1056–1066Google Scholar
  53. Groffman PM, Kareiva P, Carter SL, Grimm NB, Lawler JJ, Mack MC, Matzek V, Tallis H (2013) Ch. 8: Ecosystems, biodiversity, and ecosystem services. In: Melillo JM, Richmond TTC, Yohe GW (eds) Climate change impacts in the United States: The Third National Climate Assessment. U.S. Global Change Researh Program.
  54. Hart SC, Nason GE, Myrold DD, Perry DA (1994) Dynamics of gross nitrogen transformations in an old-growth forest: the carbon connection. Ecology 75(4):880–891Google Scholar
  55. Henry HAL (2007) Soil freeze-thaw cycle experiments: trends, methodological weaknesses and suggested improvements. Soil Biol Biochem 39(5):977–986Google Scholar
  56. Hofmockel KS, Gallet-Budynek A, McCarthy HR, Currie WS, Jackson RB, Finzi A (2011) Sources of increased N uptake in forest trees growing under elevated CO2: results of a large-scale 15N study. Glob Change Biol 17(11):3338–3350Google Scholar
  57. Holmes RT, Likens GE (2016) Hubbard Brook: the story of a forest ecosystem. Yale University Press, New HavenGoogle Scholar
  58. Hutchinson GE (1973) Eutrophication. Am Sci 61:269–279Google Scholar
  59. Hughes JW, Fahey TJ (1994) Litterfall dynamics and ecosystem recovery during forest development. For Ecol Manag 63(2–3):181–198Google Scholar
  60. Johnson CE, Driscoll CT, Siccama TG, Likens GE (2000) Element fluxes and landscape position in a northern hardwood forest watershed ecosystem. Ecosystems 3(2):159–184Google Scholar
  61. Johnson CE, Driscoll CT, Blum JD, Fahey TJ, Battles JJ (2014) Soil chemical dynamics after calcium silicate addition to a northern hardwood forest. Soil Sci Soc Am J 78(4):1458–1468Google Scholar
  62. Judd KE, Likens GE, Groffman PM (2007) High nitrate retention during winter in soils of the Hubbard Brook experimental forest. Ecosystems 10(2):217–225Google Scholar
  63. Judd K, Likens G, Buso D, Bailey A (2011) Minimal response in watershed nitrate export to severe soil frost raises questions about nutrient dynamics in the Hubbard Brook experimental forest. Biogeochemistry 106(3):443–459Google Scholar
  64. Juice SM, Fahey TJ, Siccama TG, Driscoll CT, Denny EG, Eagar C, Cleavitt NL, Minocha R, Richardson AD (2006) Response of sugar maple to calcium addition to Northern Hardwood Forest. Ecology 87(5):1267–1280Google Scholar
  65. Keenan TF, Gray J, Friedl MA, Toomey M, Bohrer G, Hollinger DY, Munger JW, O’Keefe J, Schmid HP, Wing IS, Yang B, Richardson AD (2014) Net carbon uptake has increased through warming-induced changes in temperate forest phenology. Nat Clim Change 4(7):598–604Google Scholar
  66. Keenan TF, Prentice IC, Canadell JG, Williams CA, Wang H, Raupach M, Collatz GJ (2016) Recent pause in the growth rate of atmospheric CO2 due to enhanced terrestrial carbon uptake. Nat Commun 7:13428Google Scholar
  67. Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77(6):1716–1727Google Scholar
  68. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems in globally distributed. Ecology 89(2):371–379Google Scholar
  69. Li A, Fahey TJ (2013) Nitrogen translocation to fresh litter in northern hardwood forest. Ecosystems 16(3):521–528Google Scholar
  70. Likens GE (2013) Biogeochemistry of a forested ecosystem, 3rd edn. Springer, New YorkGoogle Scholar
  71. Likens GE, Buso DC (2012) Dilution and the elusive baseline. Environ Sci Technol 46(8):4382–4387Google Scholar
  72. Likens GE, Driscoll CT, Buso DC (1996) Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272(5259):244–246Google Scholar
  73. Liu B, Mou C, Yan G, Xu L, Jiang S, Xing Y, Han S, Yu J, Wang Q (2016) Annual soil CO2 efflux in a cold temperate forest in northeastern China: effects of winter snowpack and artificial nitrogen deposition. Sci Rep 6:18957Google Scholar
  74. Lloret J, Valiela I (2016) Unprecedented decrease in deposition of nitrogen oxides over North America: the relative effects of emission controls and prevailing air-mass trajectories. Biogeochemistry 129(1):165–180Google Scholar
  75. Loehle C, Idso C, Wigley TB (2016) Physiological and ecological factors influencing recent trends in United States forest health responses to climate change. For Ecol Manag 363:179–189Google Scholar
  76. Lovett GM, Arthur MA, Crowley KF (2016) Effects of calcium on the rate and extent of litter decomposition in a northern hardwood forest. Ecosystems 19(1):87–97Google Scholar
  77. Luo Y, Melillo J, Niu S, Beier C, Clark JS, Classen AT, Davidson E, Dukes JS, Evans RD, Field CB, Czimczik CI, Keller M, Kimball BA, Kueppers LM, Norby RJ, Pelini SL, Pendall E, Rastetter E, Six J, Smith M, Tjoelker MG, Torn MS (2011) Coordinated approaches to quantify long-term ecosystem dynamics in response to global change. Glob Change Biol 17(2):843–854Google Scholar
  78. Martin CW, Driscoll CT, Fahey TJ (2000) Changes in streamwater chemistry after 20 years from forested watersheds in New Hampshire, USA. Can J For Res 30(8):1206–1213Google Scholar
  79. Martz F, Vuosku J, Ovaskainen A, Stark S, Rautio P (2016) The snow must go on: ground ice encasement, snow compaction and absence of snow differently cause soil hypoxia, CO2 accumulation and tree seedling damage in boreal forest. PLoS ONE 11(6):e0156620Google Scholar
  80. McDowell WH, Cole JJ, Driscoll CT (1987) Simplified version of the ampoule-persulfate method for determination of dissolved organic carbon. Can J Fish Aquat Sci 44(1):214–218Google Scholar
  81. McLauchlan KK, Craine JK, Oswald WW, Leavitt PR, Likens GE (2007) Changes in nitrogen cycling during the past century in a northern heardwood forest. Proc Natl Acad Sci USA 104(18):7466–7470Google Scholar
  82. Melillo JM, Butler S, Johnson J, Mohan J, Steudler P, Lux H, Burrows E, Bowles F, Smith R, Scott L, Vario C, Hill T, Burton A, Zhou Y-M, Tang J (2011) Soil warming, carbon–nitrogen interactions, and forest carbon budgets. Proc Natl Acad Sci USA 108(23):9508–9512Google Scholar
  83. Morse JL, Werner SF, Gillen C, Bailey SW, McGuire KJ, Groffman PM (2014) Searching for biogeochemical hotspots in three dimensions: soil C and N cycling in hydropedologic units in a northern hardwood forest. J Geophys Res Biogeosci 119:1596–1607Google Scholar
  84. Morse JL, Durán J, Beall F, Enanga E, Creed IF, Fernandez IJ, Groffman PM (2015a) Soil denitrification fluxes from three northeastern North American forests across a range of nitrogen depositon. Oecologia 177:17–27Google Scholar
  85. Morse JL, Durán J, Groffman PM (2015b) Denitrification and greenhouse gas fluxes in a northern hardwood forest: the importance of snowmelt and implications for ecosystem N budgets. Ecosystems 18(3):520–532Google Scholar
  86. Muller RN, Bormann FH (1976) Role of Erythronium americanum Ker. in energy flow and nutrient dynamics of a northern hardwood forest ecosystem. Science 193:1126–1128Google Scholar
  87. Niu S, Classen AT, Dukes JS, Kardol P, Liu L, Luo Y, Rustad L, Sun J, Tang J, Templer PH, Thomas RQ, Tian D, Vicca S, Wang Y-P, Xia J, Zaehle S (2016) Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. Ecol Lett 19(6):697–709Google Scholar
  88. Oulehle F, Evans CD, Hofmeister J, Krejci R, Tahovska K, Persson T, Cudlin P, Hruska J (2011) Major changes in forest carbon and nitrogen cycling caused by declining sulphur deposition. Glob Change Biol 17(10):3115–3129Google Scholar
  89. Oulehle F, Chuman T, Hruška J, Krám P, McDowell WH, Myška O, Navrátil T, Tesař M (2017) Recovery from acidification alters concentrations and fluxes of solutes from Czech catchments. Biogeochemistry 132(3):251–272Google Scholar
  90. Pastor J, Aber JD, McClaugherty CA, Melillo JM (1984) Above-ground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65(1):256–268Google Scholar
  91. Pendall E, Rustad L, Schimel J (2008) Towards a predictive understanding of belowground process responses to climate change: have we moved any closer? Funct Ecol 22(6):937–940Google Scholar
  92. 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(2):187–194Google Scholar
  93. Reinmann AB, Templer PH, Campbell JL (2012) Severe soil frost reduces losses of carbon and nitrogen from the forest floor during simulated snowmelt: a laboratory experiment. Soil Biol Biochem 44(1):65–74Google Scholar
  94. Richardson AD, Black TA, Ciais P, Delbart N, Friedl MA, Gobron N, Hollinger DY, Kutsch WL, Longdoz B, Luyssaert S, Migliavacca M, Montagnani L, Munger JW, Moors E, Piao SL, Rebmann C, Reichstein M, Saigusa N, Tomelleri E, Vargas R, Varlagin A (2010) Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philos Trans R Soc B Biol Sci 365(1555):3227–3246Google Scholar
  95. Robertson GP, Groffman PM (2007) Nitrogen transformations. In: Paul EA (ed) Soil microbiology, ecology, and biochemistry, 3rd edn. Academic Press, New York, pp 341–364Google Scholar
  96. Robertson GP, Wedin D, Groffman PM, Blair JM, Holland EA, Nadelhoffer KA, Harris D (1999) Soil carbon and nitrogen availability: Nitrogen mineralization, nitrification and carbon turnover. In: Robertson GP, Bledsoe CS, Coleman DC, Sollins P (eds) Standard soil methods for long term ecological research. Oxford University Press, New York, pp 258–271Google Scholar
  97. Rosi-Marshall EJ, Bernhardt ES, Buso DC, Driscoll CT, Likens GE (2016) Acid rain mitigation experiment shifts a forested watershed from a net sink to a net source of nitrogen. Proc Natl Acad Sci USA 113(27):7580–7583Google Scholar
  98. Ryan DF, Bormann FH (1982) Nutrient resorption in northern hardwood forests. Bioscience 32(1):29–32Google Scholar
  99. Schwarz PA, Fahey TJ, McCulloch CE (2003) Factors controlling spatial variation of tree species abundance in a forested landscape. Ecology 84(7):1862–1878Google Scholar
  100. See CR, Yanai RD, Fisk MC, Vadeboncoeur MA, Quintero BA, Fahey TJ (2015) Soil nitrogen affects phosphorus recycling: foliar resorption and plant–soil feedbacks in a northern hardwood forest. Ecology 96(9):2488–2498Google Scholar
  101. Shao S, Driscoll CT, Johnson CE, Fahey TJ, Battles JJ, Blum JD (2016) Long-term responses in soil solution and stream-water chemistry at Hubbard Brook after experimental addition of wollastonite. Environ Chem 13(3):528–540Google Scholar
  102. Sorensen PO, Templer PH, Christenson LM, Durán J, Fahey TJ, Fisk MC, Groffman PM, Morse JL, Finzi AC (2016a) Reduction in snow cover alters root-microbe interactions and decreases nitrification in a northern hardwood forest. Ecology 97(12):3359–3368Google Scholar
  103. Sorensen PO, Templer PH, Finzi AC (2016b) Contrasting effects of winter snowpack and soil frost on growing season microbial biomass and enzyme activity in two mixed-hardwood forests. Biogeochemistry 128(1):141–154Google Scholar
  104. Sorensen PO, Finzi AC, Giasson M, Reinmann AB, Sanders-Demott R, Templer PH (2017) Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming. Soil Biol Biochem. 116:39–47Google Scholar
  105. Stoddard JL (1994) Long-term changes in watershed retention of nitrogen. In: Baker LA (ed) Environmental chemistry of lakes and reservoirs. Advances in chemistry series. American Chemical Society, Washington, pp 223–284Google Scholar
  106. Tierney GL, Fahey TJ, Groffman PM, Hardy JP, Fitzhugh RD, Driscoll CT (2001) Soil freezing alters fine root dynamics in a northern hardwood forest. Biogeochemistry 56(2):175–190Google Scholar
  107. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea—how can it occur? Biogeochemistry 13(2):87–115Google Scholar
  108. Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA, Todd RL (1979) Nitrate losses from disturbed ecosystems. Science 204:469–474Google Scholar
  109. Weih M (2000) Growth of mountain birch seedlings in early-successional patches: a year-round perspective. Plant Biol 2(04):428–436Google Scholar
  110. Weih M, Karlsson PS, Skre O (1998) Intra-specific variation in nitrogen economy among three mountain birch provenances. Ecoscience 5(1):108–116Google Scholar
  111. Wexler S, Goodale CL, McGuire KJ, Bailey SW, Groffman PM (2014) Isotopic signals of summer denitrification in a northern hardwood forested catchment. Proc Natl Acad Sci USA 111:16413–16418Google Scholar
  112. Xu Z, Jiang Y, Zhou G (2016) Nitrogen cycles in terrestrial ecosystems: climate change impacts and mitigation. Environ Rev 24(2):132–143Google Scholar
  113. Yanai RD, Vadeboncoeur MA, Hamburg SP, Arthur MA, Fuss CB, Groffman PM, Siccama TG, Driscoll CT (2013) From missing source to missing sink: long-term changes in the nitrogen budget of a northern hardwood forest. Environ Sci Technol 47(20):11440–11448Google Scholar
  114. Zak DR, Groffman PM, Pregitzer KS, Christensen S, Tiedje JM (1990) The vernal dam: plant microbe competition for nitrogen in northern hardwood forests. Ecology 71(2):651–656Google Scholar
  115. Zak DR, Holmes WE, Finzi AC, Norby RJ, Schlesinger WH (2003) Soil nitrogen cycling under elevated CO2: a synthesis of forest face experiments. Ecol Appl 13(6):1508–1514Google Scholar
  116. Zak DR, Pregitzer KS, Kubiske ME, Burton AJ (2011) Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecol Lett 14(12):1220–1226Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Peter M. Groffman
    • 1
    • 8
    Email author
  • Charles T. Driscoll
    • 2
  • Jorge Durán
    • 3
  • John L. Campbell
    • 4
  • Lynn M. Christenson
    • 5
  • Timothy J. Fahey
    • 6
  • Melany C. Fisk
    • 7
  • Colin Fuss
    • 8
  • Gene E. Likens
    • 8
  • Gary Lovett
    • 8
  • Lindsey Rustad
    • 4
  • Pamela H. Templer
    • 9
  1. 1.Advanced Science Research Center at the Graduate CenterCity University of New YorkNew YorkUSA
  2. 2.Department of Civil and Environmental EngineeringSyracuse UniversitySyracuseUSA
  3. 3.Department of Life Sciences, Centre for Functional EcologyUniversity of CoimbraCoimbraPortugal
  4. 4.USDA Forest Service Northern Research StationDurhamUSA
  5. 5.Vassar CollegePoughkeepsieUSA
  6. 6.Department of Natural ResourcesCornell UniversityIthacaUSA
  7. 7.Department of ZoologyMiami UniversityOxfordUSA
  8. 8.Cary Institute of Ecosystem StudiesMillbrookUSA
  9. 9.Department of BiologyBoston UniversityBostonUSA

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