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

Title: Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems

ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7]; ORCiD logo [3];  [1];  [8]; ORCiD logo [1]; ORCiD logo [1]
  1. Aarhus Univ. (Denmark)
  2. Univ. of Exeter (United Kingdom)
  3. Northern Arizona Univ., Flagstaff, AZ (United States)
  4. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  5. Wageningen Univ. (Netherlands)
  6. Univ. de Alicante (Spain)
  7. Univ. of California, Riverside, CA (United States)
  8. Univ. of New Mexico, Albuquerque, NM (United States)
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA); Aarhus University Research Foundation; National Natural Science Foundation of China (NNSFC); China Postdoctoral Science Foundation; European Research Council (ERC); USDOE Laboratory Directed Research and Development (LDRD) Program; Generalitat Valenciana; European Comission (EC)
OSTI Identifier:
Alternate Identifier(s):
OSTI ID: 1635579
Report Number(s):
Journal ID: ISSN 1354-1013; 1022317
Grant/Contract Number:  
AC52-07NA27344; AUFF-E-2019-7-1; 839806; 41701292; 2017M610647; 2018T111091; 647038; CIDEGENT/2018/041; H2020-MSCA-IF-2018
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Global Change Biology
Additional Journal Information:
Journal Volume: 26; Journal Issue: 9; Journal ID: ISSN 1354-1013
Country of Publication:
United States
phosphorus limitation; nitrogen addition; soil phosphatase activity; soil nitrogen content; soil phosphorus content; soil ph; microbial biomass; nutrient stoichiometry balance

Citation Formats

Chen, Ji, Groenigen, Kees J., Hungate, Bruce A., Terrer, César, Groenigen, Jan‐Willem, Maestre, Fernando T., Ying, Samantha C., Luo, Yiqi, Jørgensen, Uffe, Sinsabaugh, Robert L., Olesen, Jørgen E., and Elsgaard, Lars. Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems. United States: N. p., 2020. Web. doi:10.1111/gcb.15218.
Chen, Ji, Groenigen, Kees J., Hungate, Bruce A., Terrer, César, Groenigen, Jan‐Willem, Maestre, Fernando T., Ying, Samantha C., Luo, Yiqi, Jørgensen, Uffe, Sinsabaugh, Robert L., Olesen, Jørgen E., & Elsgaard, Lars. Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems. United States. doi:10.1111/gcb.15218.
Chen, Ji, Groenigen, Kees J., Hungate, Bruce A., Terrer, César, Groenigen, Jan‐Willem, Maestre, Fernando T., Ying, Samantha C., Luo, Yiqi, Jørgensen, Uffe, Sinsabaugh, Robert L., Olesen, Jørgen E., and Elsgaard, Lars. Fri . "Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems". United States. doi:10.1111/gcb.15218.
title = {Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems},
author = {Chen, Ji and Groenigen, Kees J. and Hungate, Bruce A. and Terrer, César and Groenigen, Jan‐Willem and Maestre, Fernando T. and Ying, Samantha C. and Luo, Yiqi and Jørgensen, Uffe and Sinsabaugh, Robert L. and Olesen, Jørgen E. and Elsgaard, Lars},
abstractNote = {},
doi = {10.1111/gcb.15218},
journal = {Global Change Biology},
issn = {1354-1013},
number = 9,
volume = 26,
place = {United States},
year = {2020},
month = {6}

Journal Article:
Free Publicly Available Full Text
This content will become publicly available on June 12, 2021
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Soil carbon loss with warming: New evidence from carbon‐degrading enzymes
journal, April 2020

  • Chen, Ji; Elsgaard, Lars; Groenigen, Kees Jan
  • Global Change Biology, Vol. 26, Issue 4
  • DOI: 10.1111/gcb.14986

The role of sulfur- and phosphorus-mobilizing bacteria in biochar-induced growth promotion of Lolium perenne
journal, July 2014

  • Fox, Aaron; Kwapinski, Witold; Griffiths, Bryan S.
  • FEMS Microbiology Ecology, Vol. 90, Issue 1
  • DOI: 10.1111/1574-6941.12374

Resource stoichiometry and the biogeochemical consequences of nitrogen deposition in a mixed deciduous forest
journal, December 2016

  • Midgley, Meghan G.; Phillips, Richard P.
  • Ecology, Vol. 97, Issue 12
  • DOI: 10.1002/ecy.1595

Soilaluminum, Iron, and Phosphorus Dynamics in Response to Long-Term Experimental Nitrogen and Sulfur Additions at the Bear Brook Watershed in Maine, USA
journal, June 2006

  • Sherman, Jessica; Fernandez, Ivan J.; Norton, Stephen A.
  • Environmental Monitoring and Assessment, Vol. 121, Issue 1-3
  • DOI: 10.1007/s10661-005-9140-2

ECOLOGY: Controlling Eutrophication: Nitrogen and Phosphorus
journal, February 2009

Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies
journal, October 2008

Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems
journal, November 2011

Resource limitation is a driver of local adaptation in mycorrhizal symbioses
journal, January 2010

  • Johnson, N. C.; Wilson, G. W. T.; Bowker, M. A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
  • DOI: 10.1073/pnas.0906710107

Phosphorus in Soils of Temperate Forests: Linkages to Acidity and Aluminum
journal, November 2010

  • SanClements, Michael D.; Fernandez, Ivan J.; Norton, Stephen A.
  • Soil Science Society of America Journal, Vol. 74, Issue 6
  • DOI: 10.2136/sssaj2009.0267

Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance
journal, March 2013

  • Kuzyakov, Yakov; Xu, Xingliang
  • New Phytologist, Vol. 198, Issue 3
  • DOI: 10.1111/nph.12235

Plant nutrient-acquisition strategies change with soil age
journal, February 2008

Incorporating phosphorus cycling into global modeling efforts: a worthwhile, tractable endeavor
journal, June 2015

  • Reed, Sasha C.; Yang, Xiaojuan; Thornton, Peter E.
  • New Phytologist, Vol. 208, Issue 2
  • DOI: 10.1111/nph.13521

Water management to mitigate the global warming potential of rice systems: A global meta-analysis
journal, March 2019

Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review
journal, January 2015

Global patterns of phosphatase activity in natural soils
journal, May 2017

Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes
journal, May 2019

  • Tedersoo, Leho; Bahram, Mohammad
  • Biological Reviews, Vol. 94, Issue 5
  • DOI: 10.1111/brv.12538

Pervasive phosphorus limitation of tree species but not communities in tropical forests
journal, March 2018

  • Turner, Benjamin L.; Brenes-Arguedas, Tania; Condit, Richard
  • Nature, Vol. 555, Issue 7696
  • DOI: 10.1038/nature25789

Opportunities for mobilizing recalcitrant phosphorus from agricultural soils: a review
journal, August 2017

  • Menezes-Blackburn, Daniel; Giles, Courtney; Darch, Tegan
  • Plant and Soil, Vol. 427, Issue 1-2
  • DOI: 10.1007/s11104-017-3362-2

Evolution of the global phosphorus cycle
journal, December 2016

  • Reinhard, Christopher T.; Planavsky, Noah J.; Gill, Benjamin C.
  • Nature, Vol. 541, Issue 7637
  • DOI: 10.1038/nature20772

Global change effects on humid tropical forests: Evidence for biogeochemical and biodiversity shifts at an ecosystem scale: Tropical Forests and Global Change
journal, August 2016

  • Cusack, Daniela F.; Karpman, Jason; Ashdown, Daniel
  • Reviews of Geophysics, Vol. 54, Issue 3
  • DOI: 10.1002/2015RG000510

Nature of Phosphorus Limitation in the Ultraoligotrophic Eastern Mediterranean
journal, August 2005

Costimulation of soil glycosidase activity and soil respiration by nitrogen addition
journal, July 2016

  • Chen, Ji; Luo, Yiqi; Li, Jianwei
  • Global Change Biology, Vol. 23, Issue 3
  • DOI: 10.1111/gcb.13402

Soil Microorganisms Mediating Phosphorus Availability Update on Microbial Phosphorus
journal, May 2011

  • Richardson, Alan E.; Simpson, Richard J.
  • Plant Physiology, Vol. 156, Issue 3
  • DOI: 10.1104/pp.111.175448

Opportunities for improving phosphorus-use efficiency in crop plants: Tansley review
journal, June 2012

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

Stoichiometry of soil enzyme activity at global scale: Stoichiometry of soil enzyme activity
journal, September 2008

Mycorrhizal association as a primary control of the CO 2 fertilization effect
journal, June 2016

Effects of long-term fertilization on peat stoichiometry and associated microbial enzyme activity in an ombrotrophic bog
journal, July 2016

  • Pinsonneault, Andrew J.; Moore, Tim R.; Roulet, Nigel T.
  • Biogeochemistry, Vol. 129, Issue 1-2
  • DOI: 10.1007/s10533-016-0224-6

Stronger warming effects on microbial abundances in colder regions
journal, December 2015

  • Chen, Ji; Luo, Yiqi; Xia, Jianyang
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep18032

Soil microbial community structure and enzymatic activity responses to nitrogen management and landscape positions in switchgrass ( Panicum virgatum L.)
journal, January 2019

  • Sekaran, Udayakumar; McCoy, Cameron; Kumar, Sandeep
  • GCB Bioenergy, Vol. 11, Issue 7
  • DOI: 10.1111/gcbb.12591

WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas: NEW CLIMATE SURFACES FOR GLOBAL LAND AREAS
journal, May 2017

  • Fick, Stephen E.; Hijmans, Robert J.
  • International Journal of Climatology, Vol. 37, Issue 12
  • DOI: 10.1002/joc.5086

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

Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources
journal, January 2014

  • Mooshammer, Maria; Wanek, Wolfgang; Zechmeister-Boltenstern, Sophie
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00022

Nitrogen Saturation in Temperate Forest Ecosystems
journal, November 1998

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

Impact of long-term nitrogen addition on carbon stocks in trees and soils in northern Europe
journal, June 2007

glmulti : An R Package for Easy Automated Model Selection with (Generalized) Linear Models
journal, January 2010

  • Calcagno, Vincent; Mazancourt, Claire de
  • Journal of Statistical Software, Vol. 34, Issue 12
  • DOI: 10.18637/jss.v034.i12

Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems
journal, December 2007

Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems
journal, October 2013

  • Wei, Cunzheng; Yu, Qiang; Bai, Edith
  • Global Change Biology, Vol. 19, Issue 12
  • DOI: 10.1111/gcb.12348

Plant and microbial responses to nitrogen and phosphorus addition across an elevational gradient in subarctic tundra
journal, July 2014

  • Sundqvist, Maja K.; Liu, Zhanfeng; Giesler, Reiner
  • Ecology, Vol. 95, Issue 7
  • DOI: 10.1890/13-0869.1

A meta-analysis of 1,119 manipulative experiments on terrestrial carbon-cycling responses to global change
journal, August 2019

Conducting Meta-Analyses in R with the metafor Package
journal, January 2010

A keystone microbial enzyme for nitrogen control of soil carbon storage
journal, August 2018

Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions
journal, May 2008

Through form to function: root hair development and nutrient uptake
journal, February 2000

Microbial carbon limitation: The need for integrating microorganisms into our understanding of ecosystem carbon cycling
journal, April 2020

  • Soong, Jennifer L.; Fuchslueger, Lucia; Marañon‐Jimenez, Sara
  • Global Change Biology, Vol. 26, Issue 4
  • DOI: 10.1111/gcb.14962

Amazon forest response to CO2 fertilization dependent on plant phosphorus acquisition
journal, August 2019

Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization
journal, February 2018

  • Carrara, Joseph E.; Walter, Christopher A.; Hawkins, Jennifer S.
  • Global Change Biology, Vol. 24, Issue 6
  • DOI: 10.1111/gcb.14081

Physiological functions of mineral macronutrients
journal, June 2009

Towards a more physiological representation of vegetation phosphorus processes in land surface models
journal, February 2019

  • Jiang, Mingkai; Caldararu, Silvia; Zaehle, Sönke
  • New Phytologist, Vol. 222, Issue 3
  • DOI: 10.1111/nph.15688

Competition between plant and bacterial cells at the microscale regulates the dynamics of nitrogen acquisition in wheat ( Triticum aestivum )
journal, July 2013

  • Jones, David L.; Clode, Peta L.; Kilburn, Matt R.
  • New Phytologist, Vol. 200, Issue 3
  • DOI: 10.1111/nph.12405

Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis
journal, October 2016

A meta-analysis of soil extracellular enzyme activities in response to global change
journal, August 2018

Metabolic Adaptations of Phosphate-Starved Plants
journal, May 2011

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

Teasing apart plant community responses to N enrichment: the roles of resource limitation, competition and soil microbes
journal, August 2016

  • Farrer, Emily C.; Suding, Katharine N.
  • Ecology Letters, Vol. 19, Issue 10
  • DOI: 10.1111/ele.12665

The Meta-Analysis of Response Ratios in Experimental Ecology
journal, June 1999

Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource
journal, March 2003

The phosphorus status of northern hardwoods differs by species but is unaffected by nitrogen fertilization
journal, September 2009

Long-term research in ecology and evolution: a survey of challenges and opportunities
journal, February 2018

  • Kuebbing, Sara E.; Reimer, Adam P.; Rosenthal, Seth A.
  • Ecological Monographs, Vol. 88, Issue 2
  • DOI: 10.1002/ecm.1289

Nitrogen and phosphorus regulation of soil enzyme activities in acid forest soils
journal, July 2016

Global‐scale impacts of nitrogen deposition on tree carbon sequestration in tropical, temperate, and boreal forests: A meta‐analysis
journal, September 2017

  • Schulte‐Uebbing, Lena; de Vries, Wim
  • Global Change Biology, Vol. 24, Issue 2
  • DOI: 10.1111/gcb.13862

Diagnosing phosphorus limitations in natural terrestrial ecosystems in carbon cycle models
journal, July 2017

Global evidence on nitrogen saturation of terrestrial ecosystem net primary productivity
journal, February 2016

Differential responses of carbon-degrading enzyme activities to warming: Implications for soil respiration
journal, August 2018

  • Chen, Ji; Luo, Yiqi; García-Palacios, Pablo
  • Global Change Biology, Vol. 24, Issue 10
  • DOI: 10.1111/gcb.14394

Classification of natural communities
journal, January 1962

Decoupling of soil nutrient cycles as a function of aridity in global drylands
journal, October 2013

  • Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Gallardo, Antonio
  • Nature, Vol. 502, Issue 7473
  • DOI: 10.1038/nature12670

Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest
journal, August 2011

  • Wright, S. Joseph; Yavitt, Joseph B.; Wurzburger, Nina
  • Ecology, Vol. 92, Issue 8
  • DOI: 10.1890/10-1558.1

The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860
journal, August 2009

  • Davidson, Eric A.
  • Nature Geoscience, Vol. 2, Issue 9
  • DOI: 10.1038/ngeo608

Root microbiota drive direct integration of phosphate stress and immunity
journal, March 2017

  • Castrillo, Gabriel; Teixeira, Paulo José Pereira Lima; Paredes, Sur Herrera
  • Nature, Vol. 543, Issue 7646
  • DOI: 10.1038/nature21417

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

Microbial enzyme activity at the watershed scale: response to chronic nitrogen deposition and acute phosphorus enrichment
journal, June 2013

  • Mineau, Madeleine M.; Fatemi, Farrah R.; Fernandez, Ivan J.
  • Biogeochemistry, Vol. 117, Issue 1
  • DOI: 10.1007/s10533-013-9869-6

Chronic Nitrogen Enrichment at the Watershed Scale Does Not Enhance Microbial Phosphorus Limitation
journal, April 2017

Future productivity and carbon storage limited by terrestrial nutrient availability
journal, April 2015

  • Wieder, William R.; Cleveland, Cory C.; Smith, W. Kolby
  • Nature Geoscience, Vol. 8, Issue 6
  • DOI: 10.1038/ngeo2413