Carbon cost of plant nitrogen acquisition: global carbon cycle impact from an improved plant nitrogen cycle in the Community Land Model
Abstract
Abstract Plants typically expend a significant portion of their available carbon ( C ) on nutrient acquisition – C that could otherwise support growth. However, given that most global terrestrial biosphere models ( TBM s) do not include the C cost of nutrient acquisition, these models fail to represent current and future constraints to the land C sink. Here, we integrated a plant productivity‐optimized nutrient acquisition model – the Fixation and Uptake of Nitrogen Model – into one of the most widely used TBM s, the Community Land Model. Global plant nitrogen ( N ) uptake is dynamically simulated in the coupled model based on the C costs of N acquisition from mycorrhizal roots, nonmycorrhizal roots, N‐fixing microbes, and retranslocation (from senescing leaves). We find that at the global scale, plants spend 2.4 Pg C yr −1 to acquire 1.0 Pg N yr −1 , and that the C cost of N acquisition leads to a downregulation of global net primary production ( NPP ) by 13%. Mycorrhizal uptake represented the dominant pathway by which N is acquired, accounting for ~66% of the N uptake by plants. Notably, roots associating with arbuscular mycorrhizal ( AM ) fungi – generally considered for their rolemore »
- Authors:
-
- Jet Propulsion Laboratory California Institute of Technology 4800 Oak Grove Drive Pasadena CA 91109 USA, Joint Institute for Regional Earth System Science and Engineering University of California at Los Angeles Los Angeles CA 90095 USA
- Department of Biology West Virginia University 53 Campus Drive Morgantown WV 26506 USA
- Department of Biology Indiana University 702 N. Walnut Grove Avenue Bloomington IN 47405 USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1400935
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Global Change Biology
- Additional Journal Information:
- Journal Name: Global Change Biology Journal Volume: 22 Journal Issue: 3; Journal ID: ISSN 1354-1013
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Shi, Mingjie, Fisher, Joshua B., Brzostek, Edward R., and Phillips, Richard P. Carbon cost of plant nitrogen acquisition: global carbon cycle impact from an improved plant nitrogen cycle in the Community Land Model. United Kingdom: N. p., 2016.
Web. doi:10.1111/gcb.13131.
Shi, Mingjie, Fisher, Joshua B., Brzostek, Edward R., & Phillips, Richard P. Carbon cost of plant nitrogen acquisition: global carbon cycle impact from an improved plant nitrogen cycle in the Community Land Model. United Kingdom. https://doi.org/10.1111/gcb.13131
Shi, Mingjie, Fisher, Joshua B., Brzostek, Edward R., and Phillips, Richard P. Wed .
"Carbon cost of plant nitrogen acquisition: global carbon cycle impact from an improved plant nitrogen cycle in the Community Land Model". United Kingdom. https://doi.org/10.1111/gcb.13131.
@article{osti_1400935,
title = {Carbon cost of plant nitrogen acquisition: global carbon cycle impact from an improved plant nitrogen cycle in the Community Land Model},
author = {Shi, Mingjie and Fisher, Joshua B. and Brzostek, Edward R. and Phillips, Richard P.},
abstractNote = {Abstract Plants typically expend a significant portion of their available carbon ( C ) on nutrient acquisition – C that could otherwise support growth. However, given that most global terrestrial biosphere models ( TBM s) do not include the C cost of nutrient acquisition, these models fail to represent current and future constraints to the land C sink. Here, we integrated a plant productivity‐optimized nutrient acquisition model – the Fixation and Uptake of Nitrogen Model – into one of the most widely used TBM s, the Community Land Model. Global plant nitrogen ( N ) uptake is dynamically simulated in the coupled model based on the C costs of N acquisition from mycorrhizal roots, nonmycorrhizal roots, N‐fixing microbes, and retranslocation (from senescing leaves). We find that at the global scale, plants spend 2.4 Pg C yr −1 to acquire 1.0 Pg N yr −1 , and that the C cost of N acquisition leads to a downregulation of global net primary production ( NPP ) by 13%. Mycorrhizal uptake represented the dominant pathway by which N is acquired, accounting for ~66% of the N uptake by plants. Notably, roots associating with arbuscular mycorrhizal ( AM ) fungi – generally considered for their role in phosphorus (P) acquisition – are estimated to be the primary source of global plant N uptake owing to the dominance of AM ‐associated plants in mid‐ and low‐latitude biomes. Overall, our coupled model improves the representations of NPP downregulation globally and generates spatially explicit patterns of belowground C allocation, soil N uptake, and N retranslocation at the global scale. Such model improvements are critical for predicting how plant responses to altered N availability (owing to N deposition, rising atmospheric CO 2 , and warming temperatures) may impact the land C sink.},
doi = {10.1111/gcb.13131},
journal = {Global Change Biology},
number = 3,
volume = 22,
place = {United Kingdom},
year = {Wed Jan 06 00:00:00 EST 2016},
month = {Wed Jan 06 00:00:00 EST 2016}
}
https://doi.org/10.1111/gcb.13131
Web of Science
Works referenced in this record:
Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model
journal, January 2009
- Thornton, P. E.; Doney, S. C.; Lindsay, K.
- Biogeosciences, Vol. 6, Issue 10
The Community Climate System Model Version 4
journal, October 2011
- Gent, Peter R.; Danabasoglu, Gokhan; Donner, Leo J.
- Journal of Climate, Vol. 24, Issue 19
A comprehensive benchmarking system for evaluating global vegetation models
journal, January 2013
- Kelley, D. I.; Prentice, I. C.; Harrison, S. P.
- Biogeosciences, Vol. 10, Issue 5
Integrating plant-soil interactions into global carbon cycle models
journal, September 2009
- Ostle, Nicholas J.; Smith, Pete; Fisher, Rosie
- Journal of Ecology, Vol. 97, Issue 5
Evaluating Aspects of the Community Land and Atmosphere Models (CLM3 and CAM3) Using a Dynamic Global Vegetation Model
journal, June 2006
- Bonan, Gordon B.; Levis, Samuel
- Journal of Climate, Vol. 19, Issue 11
Modeling the carbon cost of plant nitrogen acquisition: Mycorrhizal trade-offs and multipath resistance uptake improve predictions of retranslocation: Carbon cost of mycorrhizae
journal, August 2014
- Brzostek, Edward R.; Fisher, Joshua B.; Phillips, Richard P.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 8
Multi-model mean nitrogen and sulfur deposition from the Atmospheric Chemistry and Climate Model Intercomparison Project (ACCMIP): evaluation of historical and projected future changes
journal, January 2013
- Lamarque, J. -F.; Dentener, F.; McConnell, J.
- Atmospheric Chemistry and Physics, Vol. 13, Issue 16
A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere
journal, January 2010
- Wang, Y. P.; Law, R. M.; Pak, B.
- Biogeosciences, Vol. 7, Issue 7
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
Nitrogen feedbacks increase future terrestrial ecosystem carbon uptake in an individual-based dynamic vegetation model
journal, January 2014
- Wårlind, D.; Smith, B.; Hickler, T.
- Biogeosciences, Vol. 11, Issue 21
Improving canopy processes in the Community Land Model version 4 (CLM4) using global flux fields empirically inferred from FLUXNET data
journal, January 2011
- Bonan, Gordon B.; Lawrence, Peter J.; Oleson, Keith W.
- Journal of Geophysical Research, Vol. 116, Issue G2
Influence of carbon-nitrogen cycle coupling on land model response to CO 2 fertilization and climate variability : INFLUENCE OF CARBON-NITROGEN COUPLING
journal, December 2007
- Thornton, Peter E.; Lamarque, Jean-François; Rosenbloom, Nan A.
- Global Biogeochemical Cycles, Vol. 21, Issue 4
A framework of benchmarking land models
journal, January 2012
- Luo, Y. Q.; Randerson, J.; Abramowitz, G.
- Biogeosciences Discussions, Vol. 9, Issue 2
Resource Optimization and Symbiotic Nitrogen Fixation
journal, July 2001
- Rastetter, E. B.; Vitousek, P. M.; Field, C.
- Ecosystems, Vol. 4, Issue 4
Spin-up processes in the Community Land Model version 4 with explicit carbon and nitrogen components
journal, August 2013
- Shi, Mingjie; Yang, Zong-Liang; Lawrence, David M.
- Ecological Modelling, Vol. 263
Towards an ecological understanding of biological nitrogen fixation
journal, January 2002
- Vitousek, Peter M.; Cassman, Ken; Cleveland, Cory
- Biogeochemistry, Vol. 57, Issue 1, p. 1-45
Dissolved organic nitrogen uptake by plants—an important N uptake pathway?
journal, March 2005
- Jones, David L.; Healey, John R.; Willett, Victoria B.
- Soil Biology and Biochemistry, Vol. 37, Issue 3
Nitrogen Controls on Climate Model Evapotranspiration
journal, February 2002
- Dickinson, Robert E.; Berry, Joseph A.; Bonan, Gordon B.
- Journal of Climate, Vol. 15, Issue 3
Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate
journal, July 2010
- Beer, C.; Reichstein, M.; Tomelleri, E.
- Science, Vol. 329, Issue 5993
The North American Carbon Program Multi-Scale Synthesis and Terrestrial Model Intercomparison Project – Part 1: Overview and experimental design
journal, January 2013
- Huntzinger, D. N.; Schwalm, C.; Michalak, A. M.
- Geoscientific Model Development, Vol. 6, Issue 6
Nitrogen limitation on land and in the sea: How can it occur?
journal, January 1991
- Vitousek, PeterM.; Howarth, RobertW.
- Biogeochemistry, Vol. 13, Issue 2
Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil
journal, June 2002
- Högberg, Mona N.; Högberg, Peter
- New Phytologist, Vol. 154, Issue 3
Nutrient availability as the key regulator of global forest carbon balance
journal, April 2014
- Fernández-Martínez, M.; Vicca, S.; Janssens, I. A.
- Nature Climate Change, Vol. 4, Issue 6
Ecosystem constraints to symbiotic nitrogen fixers: A simple model and its implications
journal, July 1999
- Vitousek, Peter M.; Field, Christopher B.
- Biogeochemistry, Vol. 46, Issue 1-3
Patterns and regulation of mycorrhizal plant and fungal diversity
journal, March 1995
- Allen, Edith B.; Allen, Michael F.; Helm, Dot J.
- Plant and Soil, Vol. 170, Issue 1
Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle
journal, May 2014
- Sullivan, B. W.; Smith, W. K.; Townsend, A. R.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
Diagnosing errors in a land surface model (CABLE) in the time and frequency domains
journal, January 2011
- Wang, Ying Ping; Kowalczyk, Eva; Leuning, Ray
- Journal of Geophysical Research, Vol. 116, Issue G1
Patterns of new versus recycled primary production in the terrestrial biosphere
journal, July 2013
- Cleveland, C. C.; Houlton, B. Z.; Smith, W. K.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 31
The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests
journal, April 2013
- Phillips, Richard P.; Brzostek, Edward; Midgley, Meghan G.
- New Phytologist, Vol. 199, Issue 1
Simulation of Global Land Surface Conditions from 1948 to 2004. Part I: Forcing Data and Evaluations
journal, October 2006
- Qian, Taotao; Dai, Aiguo; Trenberth, Kevin E.
- Journal of Hydrometeorology, Vol. 7, Issue 5
A unifying framework for dinitrogen fixation in the terrestrial biosphere
journal, June 2008
- Houlton, Benjamin Z.; Wang, Ying-Ping; Vitousek, Peter M.
- Nature, Vol. 454, Issue 7202
Interspecies differences in the preference of ammonium and nitrate in vascular plants
journal, January 1995
- Falkengren-Grerup, Ursula
- Oecologia, Vol. 102, Issue 3
Modeling the Terrestrial Biosphere
journal, October 2014
- Fisher, Joshua B.; Huntzinger, Deborah N.; Schwalm, Christopher R.
- Annual Review of Environment and Resources, Vol. 39, Issue 1
An Improved Canopy Integration Scheme for a Land Surface Model with Prognostic Canopy Structure
journal, August 2007
- Thornton, Peter E.; Zimmermann, Niklaus E.
- Journal of Climate, Vol. 20, Issue 15
Global soil carbon projections are improved by modelling microbial processes
journal, July 2013
- Wieder, William R.; Bonan, Gordon B.; Allison, Steven D.
- Nature Climate Change, Vol. 3, Issue 10
The Nitrogen Paradox in Tropical Forest Ecosystems
journal, December 2009
- Hedin, Lars O.; Brookshire, E. N. Jack; Menge, Duncan N. L.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 40, Issue 1
Terrestrial nitrogen feedbacks may accelerate future climate change: CARBON-NITROGEN FEEDBACKS AFFECT CLIMATE
journal, January 2010
- Zaehle, Sönke; Friedlingstein, Pierre; Friend, Andrew D.
- Geophysical Research Letters, Vol. 37, Issue 1
Implications of incorporating N cycling and N limitations on primary production in an individual-based dynamic vegetation model
journal, January 2014
- Smith, B.; Wårlind, D.; Arneth, A.
- Biogeosciences, Vol. 11, Issue 7
Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning
journal, August 2004
- Leake, Jonathan; Johnson, David; Donnelly, Damian
- Canadian Journal of Botany, Vol. 82, Issue 8
Sensitivity of inferred climate model skill to evaluation decisions: a case study using CMIP5 evapotranspiration
journal, May 2013
- Schwalm, Christopher R.; Huntinzger, Deborah N.; Michalak, Anna M.
- Environmental Research Letters, Vol. 8, Issue 2
Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest
journal, January 2015
- Brzostek, Edward R.; Dragoni, Danilo; Brown, Zachary A.
- New Phytologist, Vol. 206, Issue 4
Evaluation of 11 terrestrial carbon-nitrogen cycle models against observations from two temperate Free-Air CO 2 Enrichment studies
journal, January 2014
- Zaehle, Sönke; Medlyn, Belinda E.; De Kauwe, Martin G.
- New Phytologist, Vol. 202, Issue 3
The Community Land Model and Its Climate Statistics as a Component of the Community Climate System Model
journal, June 2006
- Dickinson, Robert E.; Oleson, Keith W.; Bonan, Gordon
- Journal of Climate, Vol. 19, Issue 11
Modeling and measuring the effects of disturbance history and climate on carbon and water budgets in evergreen needleleaf forests
journal, December 2002
- Thornton, P. E.; Law, B. E.; Gholz, Henry L.
- Agricultural and Forest Meteorology, Vol. 113, Issue 1-4
An initial intercomparison of micrometeorological and ecological inventory estimates of carbon exchange in a mid-latitude deciduous forest
journal, June 2002
- Ehman, J. L.; Schmid, H. P.; Grimmond, C. S. B.
- Global Change Biology, Vol. 8, Issue 6
Bright autumn colours of deciduous trees attract aphids: nutrient retranslocation hypothesis
journal, October 2002
- Holopainen, Jarmo K.; Peltonen, Petri
- Oikos, Vol. 99, Issue 1
Seasonal nutrient transfers by foliar resorption, leaching, and litter fall in a northern hardwood forest at Lake Clair Watershed, Quebec, Canada
journal, February 2001
- Duchesne, Louis; Ouimet, Rock; Camiré, Claude
- Canadian Journal of Forest Research, Vol. 31, Issue 2
Carbon Allocation to Ectomycorrhizal Fungi Correlates with Belowground Allocation in Culture Studies
journal, March 2006
- Hobbie, Erik A.
- Ecology, Vol. 87, Issue 3
Fertile forests produce biomass more efficiently: Forests’ biomass production efficiency
journal, April 2012
- Vicca, S.; Luyssaert, S.; Peñuelas, J.
- Ecology Letters, Vol. 15, Issue 6
Ecosystem model spin-up: Estimating steady state conditions in a coupled terrestrial carbon and nitrogen cycle model
journal, November 2005
- Thornton, Peter E.; Rosenbloom, Nan A.
- Ecological Modelling, Vol. 189, Issue 1-2
Nitrogen and phosphorous limitation reduces the effects of land use change on land carbon uptake or emission
journal, January 2015
- Wang, Ying-Ping; Zhang, Qian; Pitman, Andrew J.
- Environmental Research Letters, Vol. 10, Issue 1
Carbon cost of plant nitrogen acquisition: A mechanistic, globally applicable model of plant nitrogen uptake, retranslocation, and fixation: CARBON COST OF PLANT N ACQUISITION
journal, March 2010
- Fisher, J. B.; Sitch, S.; Malhi, Y.
- Global Biogeochemical Cycles, Vol. 24, Issue 1
Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2
journal, November 2014
- Sulman, Benjamin N.; Phillips, Richard P.; Oishi, A. Christopher
- Nature Climate Change, Vol. 4, Issue 12
RESPONSES OF N-LIMITED ECOSYSTEMS TO INCREASED CO 2 : A BALANCED-NUTRITION, COUPLED-ELEMENT-CYCLES MODEL
journal, May 1997
- Rastetter, Edward B.; Ågren, Göran I.; Shaver, Gaius R.
- Ecological Applications, Vol. 7, Issue 2
Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world
journal, June 2010
- Millard, P.; Grelet, G. -a.
- Tree Physiology, Vol. 30, Issue 9
The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts
journal, May 2010
- Courty, Pierre-Emmanuel; Buée, Marc; Diedhiou, Abdala Gamby
- Soil Biology and Biochemistry, Vol. 42, Issue 5
Nonstructural Carbon in Woody Plants
journal, April 2014
- Dietze, Michael C.; Sala, Anna; Carbone, Mariah S.
- Annual Review of Plant Biology, Vol. 65, Issue 1
The effect of vertically resolved soil biogeochemistry and alternate soil C and N models on C dynamics of CLM4
journal, January 2013
- Koven, C. D.; Riley, W. J.; Subin, Z. M.
- Biogeosciences, Vol. 10, Issue 11
Resource Limitation in Plants-An Economic Analogy
journal, November 1985
- Bloom, A. J.; Chapin, F. S.; Mooney, H. A.
- Annual Review of Ecology and Systematics, Vol. 16, Issue 1
A model of biogeochemical cycles of carbon, nitrogen, and phosphorus including symbiotic nitrogen fixation and phosphatase production: A BIOGEOCHEMICAL MODEL OF C, N, AND P
journal, March 2007
- Wang, Y. -P.; Houlton, B. Z.; Field, C. B.
- Global Biogeochemical Cycles, Vol. 21, Issue 1
Quantitative assessment of the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling
journal, May 2015
- Soudzilovskaia, Nadejda A.; Heijden, Marcel G. A.; Cornelissen, Johannes H. C.
- New Phytologist, Vol. 208, Issue 1
Leaf demography and the seasonal internal cycling of nitrogen in sycamore (Acer pseudoplatanus L.) seedlings in relation to nitrogen supply
journal, April 1991
- Millard, P.; Proe, M. F.
- New Phytologist, Vol. 117, Issue 4
Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests
journal, September 2015
- Waring, Bonnie G.; Adams, Rachel; Branco, Sara
- New Phytologist, Vol. 209, Issue 2
Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species
journal, February 2003
- Wright, I. J.; Westoby, M.
- Functional Ecology, Vol. 17, Issue 1
Parameterization improvements and functional and structural advances in Version 4 of the Community Land Model
journal, January 2011
- Lawrence, David M.; Oleson, Keith W.; Flanner, Mark G.
- Journal of Advances in Modeling Earth Systems, Vol. 3, Issue 3
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
The role of phosphorus dynamics in tropical forests – a modeling study using CLM-CNP
journal, January 2014
- Yang, X.; Thornton, P. E.; Ricciuto, D. M.
- Biogeosciences, Vol. 11, Issue 6
Global nutrient limitation in terrestrial vegetation: GLOBAL NUTRIENT LIMITATION IN VEGETATION
journal, August 2012
- Fisher, Joshua B.; Badgley, Grayson; Blyth, Eleanor
- Global Biogeochemical Cycles, Vol. 26, Issue 3
Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient
journal, September 2001
- Nordin, Annika; Högberg, Peter; Näsholm, Torgny
- Oecologia, Vol. 129, Issue 1
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
Global patterns of land-atmosphere fluxes of carbon dioxide, latent heat, and sensible heat derived from eddy covariance, satellite, and meteorological observations
journal, January 2011
- Jung, Martin; Reichstein, Markus; Margolis, Hank A.
- Journal of Geophysical Research, Vol. 116