skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle

Abstract

Nitrogen (N) deposition is impacting the services that ecosystems provide to humanity. However, the mechanisms determining impacts on the N cycle are not fully understood. To explore the mechanistic underpinnings of N impacts on N cycle processes, we reviewed and synthesised recent progress in ecosystem N research through empirical studies, conceptual analysis and model simulations. Experimental and observational studies have revealed that the stimulation of plant N uptake and soil retention generally diminishes as N loading increases, while dissolved and gaseous losses of N occur at low N availability but increase exponentially and become the dominant fate of N at high loading rates. The original N saturation hypothesis emphasises sequential N saturation from plant uptake to soil retention before N losses occur. However, biogeochemical models that simulate simultaneous competition for soil N substrates by multiple processes match the observed patterns of N losses better than models based on sequential competition. Here to enable better prediction of terrestrial N cycle responses to N loading, we recommend that future research identifies the response functions of different N processes to substrate availability using manipulative experiments, and incorporates the measured N saturation response functions into conceptual, theoretical and quantitative analyses.

Authors:
 [1];  [2];  [3];  [4];  [1];  [5];  [6];  [1];  [7];  [8];  [9];  [1];  [10];  [11];  [12];  [13]
  1. Chinese Academy of Sciences (CAS), Beijing (China)
  2. Univ. of Copenhagen, Kobenhavn (Denmark)
  3. Purdue Univ., West Lafayette, IN (United States)
  4. Swedish Univ. of Agricultural Sciences, Umea (Sweden)
  5. Univ. of Oklahoma, Norman, OK (United States)
  6. U.S. Forest Service, Durham, NH (United States)
  7. The Ecosystem Center, Woods Hole, MA (United States)
  8. Boston Univ., Boston, MA (United States)
  9. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
  10. Univ. of Antwerp, Wilrijk (Belgium)
  11. CSIRO Ocean and Atmosphere, Aspendale, VIC (Australia)
  12. East China Normal Univ., Shanghai (China);
  13. Max Planck Institute for Biogeochemistry, Jena (Germany)
Publication Date:
Research Org.:
Univ. of Tennessee, Knoxville, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1501386
Grant/Contract Number:  
SC0010562
Resource Type:
Accepted Manuscript
Journal Name:
Ecology Letters
Additional Journal Information:
Journal Volume: 19; Journal Issue: 6; Journal ID: ISSN 1461-023X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; leaching; mineralisation; nitrification; nitrogen deposition; nitrogen loss; plant N uptake; saturation; soil N retention; threshold

Citation Formats

Niu, Shuli, Classen, Aimée T., Dukes, Jeffrey S., Kardol, Paul, Liu, Lingli, Luo, Yiqi, Rustad, Lindsey, Sun, Jian, Tang, Jianwu, Templer, Pamela H., Thomas, R. Quinn, Tian, Dashuan, Vicca, Sara, Wang, Ying -Ping, Xia, Jianyang, and Zaehle, Sönke. Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. United States: N. p., 2016. Web. doi:10.1111/ele.12591.
Niu, Shuli, Classen, Aimée T., Dukes, Jeffrey S., Kardol, Paul, Liu, Lingli, Luo, Yiqi, Rustad, Lindsey, Sun, Jian, Tang, Jianwu, Templer, Pamela H., Thomas, R. Quinn, Tian, Dashuan, Vicca, Sara, Wang, Ying -Ping, Xia, Jianyang, & Zaehle, Sönke. Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. United States. doi:10.1111/ele.12591.
Niu, Shuli, Classen, Aimée T., Dukes, Jeffrey S., Kardol, Paul, Liu, Lingli, Luo, Yiqi, Rustad, Lindsey, Sun, Jian, Tang, Jianwu, Templer, Pamela H., Thomas, R. Quinn, Tian, Dashuan, Vicca, Sara, Wang, Ying -Ping, Xia, Jianyang, and Zaehle, Sönke. Wed . "Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle". United States. doi:10.1111/ele.12591. https://www.osti.gov/servlets/purl/1501386.
@article{osti_1501386,
title = {Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle},
author = {Niu, Shuli and Classen, Aimée T. and Dukes, Jeffrey S. and Kardol, Paul and Liu, Lingli and Luo, Yiqi and Rustad, Lindsey and Sun, Jian and Tang, Jianwu and Templer, Pamela H. and Thomas, R. Quinn and Tian, Dashuan and Vicca, Sara and Wang, Ying -Ping and Xia, Jianyang and Zaehle, Sönke},
abstractNote = {Nitrogen (N) deposition is impacting the services that ecosystems provide to humanity. However, the mechanisms determining impacts on the N cycle are not fully understood. To explore the mechanistic underpinnings of N impacts on N cycle processes, we reviewed and synthesised recent progress in ecosystem N research through empirical studies, conceptual analysis and model simulations. Experimental and observational studies have revealed that the stimulation of plant N uptake and soil retention generally diminishes as N loading increases, while dissolved and gaseous losses of N occur at low N availability but increase exponentially and become the dominant fate of N at high loading rates. The original N saturation hypothesis emphasises sequential N saturation from plant uptake to soil retention before N losses occur. However, biogeochemical models that simulate simultaneous competition for soil N substrates by multiple processes match the observed patterns of N losses better than models based on sequential competition. Here to enable better prediction of terrestrial N cycle responses to N loading, we recommend that future research identifies the response functions of different N processes to substrate availability using manipulative experiments, and incorporates the measured N saturation response functions into conceptual, theoretical and quantitative analyses.},
doi = {10.1111/ele.12591},
journal = {Ecology Letters},
number = 6,
volume = 19,
place = {United States},
year = {2016},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 59 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model
journal, January 2009


Short and long-term impacts of nitrogen deposition on carbon sequestration by forest ecosystems
journal, November 2014

  • de Vries, Wim; Du, Enzai; Butterbach-Bahl, Klaus
  • Current Opinion in Environmental Sustainability, Vol. 9-10
  • DOI: 10.1016/j.cosust.2014.09.001

Nitrogen saturation in a high elevation New England spruce-fir stand
journal, August 1996


Terrestrial nitrogen cycle simulation with a dynamic global vegetation model
journal, August 2008


Dynamic model of flexible phytoplankton nutrient uptake
journal, December 2011

  • Bonachela, J. A.; Raghib, M.; Levin, S. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
  • DOI: 10.1073/pnas.1118012108

Global patterns of nitrogen limitation: confronting two global biogeochemical models with observations
journal, August 2013

  • Thomas, R. Quinn; Zaehle, Sönke; Templer, Pamela H.
  • Global Change Biology, Vol. 19, Issue 10
  • DOI: 10.1111/gcb.12281

Is Nitrogen Deposition Altering the Nitrogen Status of Northeastern Forests?
journal, January 2003


Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis
journal, December 2010


Empirical Modeling of Atmospheric Deposition in Mountainous Landscapes
journal, August 2006


Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO 2 and temperature
journal, June 2012


Predicting dissolved inorganic nitrogen leaching in European forests using two independent databases
journal, February 2009


Nitrogen saturation of terrestrial ecosystems
journal, January 1988


On the fate of anthropogenic nitrogen
journal, December 2008

  • Schlesinger, W. H.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 1
  • DOI: 10.1073/pnas.0810193105

Sinks for nitrogen inputs in terrestrial ecosystems: a meta-analysis of 15 N tracer field studies
journal, August 2012

  • Templer, P. H.; Mack, M. C.; Iii, F. S. Chapin
  • Ecology, Vol. 93, Issue 8
  • DOI: 10.1890/11-1146.1

Inorganic nitrogen uptake kinetics of sugarcane (Saccharum spp.) varieties under in vitro conditions with varying N supply
journal, February 2014

  • Hajari, Elliosha; Snyman, Sandy J.; Watt, M. Paula
  • Plant Cell, Tissue and Organ Culture (PCTOC), Vol. 117, Issue 3
  • DOI: 10.1007/s11240-014-0445-0

Land use alters the resistance and resilience of soil food webs to drought
journal, January 2012

  • de Vries, Franciska T.; Liiri, Mira E.; Bjørnlund, Lisa
  • Nature Climate Change, Vol. 2, Issue 4
  • DOI: 10.1038/nclimate1368

Analyses of the impact of changes in atmospheric deposition and climate on forest growth in European monitoring plots: A stand growth approach
journal, September 2009


Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis
journal, January 2016

  • Li, Yong; Niu, Shuli; Yu, Guirui
  • Global Change Biology, Vol. 22, Issue 2
  • DOI: 10.1111/gcb.13125

Improved modelling of soil nitrogen losses
journal, July 2015


High carbon dioxide uptake by subtropical forest ecosystems in the East Asian monsoon region
journal, March 2014

  • Yu, Guirui; Chen, Zhi; Piao, Shilong
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 13
  • DOI: 10.1073/pnas.1317065111

Characterization of ammonium and nitrate uptake and assimilation in roots of tea plants
journal, December 2012

  • Yang, Y. Y.; Li, X. H.; Ratcliffe, R. G.
  • Russian Journal of Plant Physiology, Vol. 60, Issue 1
  • DOI: 10.1134/S1021443712060180

Nitrogen effects on net ecosystem carbon exchange in a temperate steppe: CARBON FLUX RESPONSES TO NITROGEN ENRICHMENT
journal, January 2010


Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions
journal, January 2010

  • Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z.
  • Ecological Applications, Vol. 20, Issue 1
  • DOI: 10.1890/08-0127.1

Biogeochemical Response of Forest Ecosystems to Simulated Chronic Nitrogen Deposition
journal, May 1997


Nitrogen regulation of the climate–carbon feedback: evidence from a long-term global change experiment
journal, November 2010

  • Niu, Shuli; Sherry, Rebecca A.; Zhou, Xuhui
  • Ecology, Vol. 91, Issue 11
  • DOI: 10.1890/09-1634.1

Nitrogen Saturation in Temperate Forest Ecosystems
journal, November 1998

  • Aber, John; McDowell, William; Nadelhoffer, Knute
  • BioScience, Vol. 48, Issue 11
  • DOI: 10.2307/1313296

Contingency in ecosystem but not plant community response to multiple global change factors
journal, August 2012


Air Pollution and Forest Decline in a Spruce (Picea abies) Forest
journal, May 1989


Does Nitrogen Constrain Carbon Cycling, or Does Carbon Input Stimulate Nitrogen Cycling? 1
journal, January 2006

  • Luo, Yiqi; Field, Christopher B.; Jackson, Robert B.
  • Ecology, Vol. 87, Issue 1
  • DOI: 10.1890/05-0923

Facultative nitrogen fixation by canopy legumes in a lowland tropical forest
journal, November 2010


Evaluating the source of streamwater nitrate using ?15N and ?18O in nitrate in two watersheds in New Hampshire, USA
journal, October 2004

  • Pardo, Linda H.; Kendall, Carol; Pett-Ridge, Jennifer
  • Hydrological Processes, Vol. 18, Issue 14
  • DOI: 10.1002/hyp.5576

Global metaanalysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen
journal, June 2014

  • Shcherbak, I.; Millar, N.; Robertson, G. P.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 25
  • DOI: 10.1073/pnas.1322434111

Regulation of Nitrate Transport in Citrus Rootstocks Depending of Nitrogen Availability
journal, September 2007

  • Cerezo, Miguel; Camañes, Gemma; Flors, Victor
  • Plant Signaling & Behavior, Vol. 2, Issue 5
  • DOI: 10.4161/psb.2.5.4578

Minor stimulation of soil carbon storage by nitrogen addition: A meta-analysis
journal, January 2011


Consequences of More Extreme Precipitation Regimes for Terrestrial Ecosystems
journal, October 2008

  • Knapp, Alan K.; Beier, Claus; Briske, David D.
  • BioScience, Vol. 58, Issue 9
  • DOI: 10.1641/B580908

Red spruce ecosystem level changes following 14 years of chronic N fertilization
journal, November 2005


Spatial changes in forest floor and foliar chemistry of spruce-fir forests across New England
journal, January 1991

  • McNulty, S. G.; Aber, J. D.; Boone, R. D.
  • Biogeochemistry, Vol. 14, Issue 1
  • DOI: 10.1007/BF00000884

The human footprint in the carbon cycle of temperate and boreal forests
journal, June 2007

  • Magnani, Federico; Mencuccini, Maurizio; Borghetti, Marco
  • Nature, Vol. 447, Issue 7146
  • DOI: 10.1038/nature05847

Extensive Management Promotes Plant and Microbial Nitrogen Retention in Temperate Grassland
journal, December 2012


Microbial denitrification dominates nitrate losses from forest ecosystems
journal, January 2015

  • Fang, Yunting; Koba, Keisuke; Makabe, Akiko
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 5
  • DOI: 10.1073/pnas.1416776112

Long-Term Nitrogen Additions and Nitrogen Saturation in Two Temperate Forests
journal, May 2000

  • Magill, Alison H.; Aber, John D.; Berntson, Glenn M.
  • Ecosystems, Vol. 3, Issue 3
  • DOI: 10.1007/s100210000023

Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe
journal, December 2013

  • Peñuelas, Josep; Poulter, Benjamin; Sardans, Jordi
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3934

Atmospheric inputs and nitrogen saturation status in and adjacent to Class I wilderness areas of the northeastern US
journal, November 2014


Crossing the threshold: the power of multi‐level experiments in identifying global change responses
journal, August 2012


Nitrogen Saturation in Northern Forest Ecosystems
journal, June 1989

  • Aber, John D.; Nadelhoffer, Knute J.; Steudler, Paul
  • BioScience, Vol. 39, Issue 6
  • DOI: 10.2307/1311067

Depolymerization and mineralization rates at 12 Mediterranean sites with varying soil N availability. A test for the Schimel and Bennett model
journal, March 2011


Modelling nitrogen saturation and carbon accumulation in heathland soils under elevated nitrogen deposition
journal, October 2006


Litter Quality and the Temperature Sensitivity of Decomposition
journal, February 2005

  • Fierer, Noah; Craine, Joseph M.; McLauchlan, Kendra
  • Ecology, Vol. 86, Issue 2
  • DOI: 10.1890/04-1254

Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China
journal, May 2009


Why is plant-growth response to elevated CO2 amplified when water is limiting, but reduced when nitrogen is limiting? A growth-optimisation hypothesis
journal, January 2008

  • McMurtrie, Ross E.; Norby, Richard J.; Medlyn, Belinda E.
  • Functional Plant Biology, Vol. 35, Issue 6
  • DOI: 10.1071/FP08128

Nitrogen limitation on land: how can it occur in Earth system models?
journal, February 2015

  • Thomas, R. Quinn; Brookshire, E. N. Jack; Gerber, Stefan
  • Global Change Biology, Vol. 21, Issue 5
  • DOI: 10.1111/gcb.12813

Modeling global annual N 2 O and NO emissions from fertilized fields : N
journal, November 2002

  • Bouwman, A. F.; Boumans, L. J. M.; Batjes, N. H.
  • Global Biogeochemical Cycles, Vol. 16, Issue 4
  • DOI: 10.1029/2001GB001812

Kinetics of ammonium and nitrate uptake by eucalypt roots and associated proton fluxes measured using ion selective microelectrodes
journal, January 2003

  • Garnett, Trevor P.; Shabala, Sergey N.; Smethurst, Philip J.
  • Functional Plant Biology, Vol. 30, Issue 11
  • DOI: 10.1071/FP03087

Global response patterns of terrestrial plant species to nitrogen addition
journal, July 2008


CO2 enhancement of forest productivity constrained by limited nitrogen availability
journal, October 2010

  • Norby, R. J.; Warren, J. M.; Iversen, C. M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 45
  • DOI: 10.1073/pnas.1006463107

Carbon–nitrogen interactions on land at global scales: current understanding in modelling climate biosphere feedbacks
journal, October 2011


Patterns of Nutrient Loss from Unpolluted, Old-Growth Temperate Forests: Evaluation of Biogeochemical Theory
journal, March 1995

  • Hedin, Lars O.; Armesto, Juan J.; Johnson, Arthur H.
  • Ecology, Vol. 76, Issue 2
  • DOI: 10.2307/1941208

A global analysis of soil acidification caused by nitrogen addition
journal, February 2015


Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide
journal, January 2004


Increased tree carbon storage in response to nitrogen deposition in the US
journal, December 2009

  • Quinn Thomas, R.; Canham, Charles D.; Weathers, Kathleen C.
  • Nature Geoscience, Vol. 3, Issue 1
  • DOI: 10.1038/ngeo721

Nitrogen Saturation and Retention in Forested Watersheds of the Catskill Mountains, new york
journal, February 2000


Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA
journal, July 2004


Soil warming, carbon-nitrogen interactions, and forest carbon budgets
journal, May 2011

  • Melillo, J. M.; Butler, S.; Johnson, J.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 23
  • DOI: 10.1073/pnas.1018189108

Nitrogen Addition Regulates Soil Nematode Community Composition through Ammonium Suppression
journal, August 2012


A New Conceptual Model of Nitrogen Saturation Based on Experimental Nitrogen Addition to an Oak Forest
journal, March 2011


Nitrogen Limitation of net Primary Productivity in Terrestrial Ecosystems is Globally Distributed
journal, February 2008

  • LeBauer, David S.; Treseder, Kathleen K.
  • Ecology, Vol. 89, Issue 2
  • DOI: 10.1890/06-2057.1

Effects of experimental nitrogen and/or phosphorus additions on soil nematode communities in a secondary tropical forest
journal, August 2014


An Earth-system perspective of the global nitrogen cycle
journal, January 2008


Symptoms of nitrogen saturation in two central Appalachian hardwood forest ecosystems
journal, December 1996

  • Peterjohn, William T.; Adams, Mary Beth; Gilliam, Frank S.
  • Biogeochemistry, Vol. 35, Issue 3
  • DOI: 10.1007/BF02183038

Effects of nitrogen saturation on tree growth and death in a mixed-oak forest
journal, May 2007


The kinetics of ammonium and nitrate uptake by young rice plants
journal, June 1982

  • Youngdahl, L. J.; Pacheco, R.; Street, J. J.
  • Plant and Soil, Vol. 69, Issue 2
  • DOI: 10.1007/BF02374517

Inhibition of Nitrate Uptake by Ammonium in Barley. Analysis of Component Fluxes
journal, May 1999

  • Kronzucker, Herbert J.; Glass, Anthony D. M.; Siddiqi, M. Yaeesh
  • Plant Physiology, Vol. 120, Issue 1
  • DOI: 10.1104/pp.120.1.283

    Works referencing / citing this record:

    A new theory of plant-microbe nutrient competition resolves inconsistencies between observations and model predictions
    journal, March 2017

    • Zhu, Qing; Riley, William J.; Tang, Jinyun
    • Ecological Applications, Vol. 27, Issue 3
    • DOI: 10.1002/eap.1490

    Nitrogen mineralization in O horizon soils during 27 years of nitrogen enrichment at the Bear Brook Watershed in Maine, USA
    journal, August 2018

    • Patel, Kaizad F.; Fernandez, Ivan J.
    • Environmental Monitoring and Assessment, Vol. 190, Issue 9
    • DOI: 10.1007/s10661-018-6945-3

    Centennial-scale reductions in nitrogen availability in temperate forests of the United States
    journal, August 2017


    Direct and indirect effects of nitrogen enrichment on soil organisms and carbon and nitrogen mineralization in a semi‐arid grassland
    journal, November 2018