Skip to main content

Advertisement

Log in

Nitrogen oligotrophication in northern hardwood forests

Biogeochemistry Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  • 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):639–648

    Google Scholar 

  • Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. Bioscience 39(6):378–386

    Google Scholar 

  • 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):375–389

    Google Scholar 

  • Andresen LC, Michelsen A (2005) Off-season uptake of nitrogen in temperate heath vegetation. Oecologia 144(4):585–597

    Google Scholar 

  • Battles JJ, Fahey TJ, Driscoll CT Jr, Blum JD, Johnson CE (2014) Restoring soil calcium reverses forest decline. Environ. Sci. Technol. Lett. 1(1):15–19

    Google Scholar 

  • Battye W, Aneja VP, Schlesinger WH (2017) Is nitrogen the next carbon? Earth’s Future 5(9):894–904

    Google Scholar 

  • 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):3406–3411

    Google Scholar 

  • 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):219–230

    Google Scholar 

  • Bohlen PJ, Groffman PM, Driscoll CT, Fahey TJ, Siccama TG (2001) Plant-soil-microbial interactions in a northern hardwood forest. Ecology 82(4):965–978

    Google Scholar 

  • Bormann FH, Likens GE (1979) Pattern and process in a forested ecosystem. Springer, New York

    Google Scholar 

  • 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):9321–9328

    Google Scholar 

  • 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):682–699

    Google Scholar 

  • 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):314–322

    Google Scholar 

  • 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, PA

  • 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):1934–1944

    Google Scholar 

  • 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):2663–2673

    Google Scholar 

  • Chapin FS, Schulze E, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21(1):423–447

    Google Scholar 

  • 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):416–434

    Google Scholar 

  • 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):82–91

    Google Scholar 

  • 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 171:261–269

    Google Scholar 

  • 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 15:1–16

    Google Scholar 

  • 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):7748–7753

    Google Scholar 

  • 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):1153–1166

    Google Scholar 

  • 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):349–357

    Google Scholar 

  • 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):180–198

    Google Scholar 

  • 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 22:1181–1188

    Google Scholar 

  • 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 146:5–14

    Google Scholar 

  • 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):3568–3577

    Google Scholar 

  • 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):e01251

    Google Scholar 

  • Elmore AJ, Nelson DM, Craine JM (2016) Earlier springs are causing reduced nitrogen availability in North American eastern deciduous forests. Nat Plants 2:16133

    Google Scholar 

  • Eshleman KN, Sabo RD, Kline KM (2013) Surface water quality is improving due to declining atmospheric N deposition. Environ Sci Technol 47(21):12193–12200

    Google Scholar 

  • Fahey TJ, Battles JJ, Wilson GF (1998) Responses of early successional northern hardwood forests to changes in nutrient availability. Ecol Monogr 68(2):183–212

    Google Scholar 

  • 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):738–744

    Google Scholar 

  • 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):2939–2947

    Google Scholar 

  • 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):1864–1873

    Google Scholar 

  • 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):215–238

    Google Scholar 

  • 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):2360–2374

    Google Scholar 

  • 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):4617–4632

    Google Scholar 

  • 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):35–47

    Google Scholar 

  • 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):889–892

    Google Scholar 

  • 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):1457–1464

    Google Scholar 

  • Goodale CL, Aber JD, Vitousek PM (2003) An unexpected nitrate decline in New Hampshire streams. Ecosystems 6(1):75–86

    Google Scholar 

  • 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):334–337

    Google Scholar 

  • 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):173–191

    Google Scholar 

  • Groffman PM, Fisk MC (2011) Calcium constrains plant control over forest ecosystem nitrogen cycling. Ecology 92:2035–2042

    Google Scholar 

  • Groffman PM, Zak DR, Christensen S, Mosier A, Tiedje JM (1993) Early spring nitrogen dynamics in a temperate forest landscape. Ecology 74(5):1579–1585

    Google Scholar 

  • 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):191–213

    Google Scholar 

  • 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):1289–1305

    Google Scholar 

  • 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):1748–1760

    Google Scholar 

  • 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 12:927–943

    Google Scholar 

  • 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):223–238

    Google Scholar 

  • 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 62:1056–1066

    Google Scholar 

  • 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. http://nca2014.globalchange.gov/report/sectors/ecosystems

  • 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):880–891

    Google Scholar 

  • Henry HAL (2007) Soil freeze-thaw cycle experiments: trends, methodological weaknesses and suggested improvements. Soil Biol Biochem 39(5):977–986

    Google Scholar 

  • 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):3338–3350

    Google Scholar 

  • Holmes RT, Likens GE (2016) Hubbard Brook: the story of a forest ecosystem. Yale University Press, New Haven

    Google Scholar 

  • Hutchinson GE (1973) Eutrophication. Am Sci 61:269–279

    Google Scholar 

  • Hughes JW, Fahey TJ (1994) Litterfall dynamics and ecosystem recovery during forest development. For Ecol Manag 63(2–3):181–198

    Google Scholar 

  • Johnson CE, Driscoll CT, Siccama TG, Likens GE (2000) Element fluxes and landscape position in a northern hardwood forest watershed ecosystem. Ecosystems 3(2):159–184

    Google Scholar 

  • 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):1458–1468

    Google Scholar 

  • Judd KE, Likens GE, Groffman PM (2007) High nitrate retention during winter in soils of the Hubbard Brook experimental forest. Ecosystems 10(2):217–225

    Google Scholar 

  • 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):443–459

    Google Scholar 

  • 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):1267–1280

    Google Scholar 

  • 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):598–604

    Google Scholar 

  • 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 7:13428

    Google Scholar 

  • Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77(6):1716–1727

    Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems in globally distributed. Ecology 89(2):371–379

    Google Scholar 

  • Li A, Fahey TJ (2013) Nitrogen translocation to fresh litter in northern hardwood forest. Ecosystems 16(3):521–528

    Google Scholar 

  • Likens GE (2013) Biogeochemistry of a forested ecosystem, 3rd edn. Springer, New York

    Google Scholar 

  • Likens GE, Buso DC (2012) Dilution and the elusive baseline. Environ Sci Technol 46(8):4382–4387

    Google Scholar 

  • Likens GE, Driscoll CT, Buso DC (1996) Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272(5259):244–246

    Google Scholar 

  • 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 6:18957

    Google Scholar 

  • 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):165–180

    Google Scholar 

  • 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 363:179–189

    Google Scholar 

  • 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):87–97

    Google Scholar 

  • 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):843–854

    Google Scholar 

  • 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):1206–1213

    Google Scholar 

  • 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):e0156620

    Google Scholar 

  • 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):214–218

    Google Scholar 

  • 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):7466–7470

    Google Scholar 

  • 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):9508–9512

    Google Scholar 

  • 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 119:1596–1607

    Google Scholar 

  • 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 177:17–27

    Google Scholar 

  • 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):520–532

    Google Scholar 

  • Muller RN, Bormann FH (1976) Role of Erythronium americanum Ker. in energy flow and nutrient dynamics of a northern hardwood forest ecosystem. Science 193:1126–1128

    Google Scholar 

  • 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):697–709

    Google Scholar 

  • 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):3115–3129

    Google Scholar 

  • 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):251–272

    Google Scholar 

  • 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):256–268

    Google Scholar 

  • 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):937–940

    Google Scholar 

  • 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):187–194

    Google Scholar 

  • 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):65–74

    Google Scholar 

  • 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):3227–3246

    Google Scholar 

  • Robertson GP, Groffman PM (2007) Nitrogen transformations. In: Paul EA (ed) Soil microbiology, ecology, and biochemistry, 3rd edn. Academic Press, New York, pp 341–364

    Google Scholar 

  • 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 258–271

    Google Scholar 

  • 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):7580–7583

    Google Scholar 

  • Ryan DF, Bormann FH (1982) Nutrient resorption in northern hardwood forests. Bioscience 32(1):29–32

    Google Scholar 

  • Schwarz PA, Fahey TJ, McCulloch CE (2003) Factors controlling spatial variation of tree species abundance in a forested landscape. Ecology 84(7):1862–1878

    Google Scholar 

  • 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):2488–2498

    Google Scholar 

  • 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):528–540

    Google Scholar 

  • 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):3359–3368

    Google Scholar 

  • 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):141–154

    Google Scholar 

  • 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. 116:39–47

    Google Scholar 

  • 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 223–284

    Google Scholar 

  • 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):175–190

    Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea—how can it occur? Biogeochemistry 13(2):87–115

    Google Scholar 

  • Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA, Todd RL (1979) Nitrate losses from disturbed ecosystems. Science 204:469–474

    Google Scholar 

  • Weih M (2000) Growth of mountain birch seedlings in early-successional patches: a year-round perspective. Plant Biol 2(04):428–436

    Google Scholar 

  • Weih M, Karlsson PS, Skre O (1998) Intra-specific variation in nitrogen economy among three mountain birch provenances. Ecoscience 5(1):108–116

    Google Scholar 

  • 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 111:16413–16418

    Google Scholar 

  • Xu Z, Jiang Y, Zhou G (2016) Nitrogen cycles in terrestrial ecosystems: climate change impacts and mitigation. Environ Rev 24(2):132–143

    Google Scholar 

  • 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):11440–11448

    Google Scholar 

  • 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):651–656

    Google Scholar 

  • 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):1508–1514

    Google Scholar 

  • 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):1220–1226

    Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter M. Groffman.

Additional information

Responsible Editor: Sujay Kaushal.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Groffman, P.M., Driscoll, C.T., Durán, J. et al. Nitrogen oligotrophication in northern hardwood forests. Biogeochemistry 141, 523–539 (2018). https://doi.org/10.1007/s10533-018-0445-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-018-0445-y

Keywords

Navigation