Processes regulating progressive nitrogen limitation under elevated carbon dioxide: a meta-analysis

Liang, Junyi; Qi, Xuan; Souza, Lara; Luo, Yiqi

doi:10.5194/bg-13-2689-2016

Processes regulating progressive nitrogen limitation under elevated carbon dioxide: a meta-analysis

Journal Article · Tue May 10 00:00:00 EDT 2016 · Biogeosciences (Online)

DOI:https://doi.org/10.5194/bg-13-2689-2016· OSTI ID:1252321

; Qi, Xuan; Souza, Lara; Luo, Yiqi

Abstract. The nitrogen (N) cycle has the potential to regulate climate change through its influence on carbon (C) sequestration. Although extensive research has explored whether or not progressive N limitation (PNL) occurs under CO2 enrichment, a comprehensive assessment of the processes that regulate PNL is still lacking. Here, we quantitatively synthesized the responses of all major processes and pools in the terrestrial N cycle with meta-analysis of CO2 experimental data available in the literature. The results showed that CO2 enrichment significantly increased N sequestration in the plant and litter pools but not in the soil pool, partially supporting one of the basic assumptions in the PNL hypothesis that elevated CO2 results in more N sequestered in organic pools. However, CO2 enrichment significantly increased the N influx via biological N fixation and the loss via N2O emission, but decreased the N efflux via leaching. In addition, no general diminished CO2 fertilization effect on plant growth was observed over time up to the longest experiment of 13 years. Overall, our analyses suggest that the extra N supply by the increased biological N fixation and decreased leaching may potentially alleviate PNL under elevated CO2 conditions in spite of the increases in plant N sequestration and N2O emission. Moreover, our syntheses indicate that CO2 enrichment increases soil ammonium (NH4+) to nitrate (NO3−) ratio. The changed NH4+/NO3− ratio and subsequent biological processes may result in changes in soil microenvironments, above-belowground community structures and associated interactions, which could potentially affect the terrestrial biogeochemical cycles. In addition, our data synthesis suggests that more long-term studies, especially in regions other than temperate ones, are needed for comprehensive assessments of the PNL hypothesis.

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Research Organization:: Univ. of Oklahoma, Norman, OK (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0004601; SC0008270; SC0010715

OSTI ID:: 1252321

Alternate ID(s):: OSTI ID: 1288361

Journal Information:: Biogeosciences (Online), Journal Name: Biogeosciences (Online) Journal Issue: 9 Vol. 13; ISSN 1726-4189

Publisher:: Copernicus Publications, EGUCopyright Statement

Country of Publication:: Germany

Language:: English

References (50)

Predicting long-term carbon sequestration in response to CO ₂ enrichment: How and why do current ecosystem models differ? Walker, Anthony P.; Zaehle, Sönke; Medlyn, Belinda E. Global Biogeochemical Cycles, Vol. 29, Issue 4 https://doi.org/10.1002/2014GB004995	journal	April 2015
Plant Physiological Ecology Lambers, Hans; Chapin, F. Stuart; Pons, Thijs L. Springer New York, NY https://doi.org/10.1007/978-0-387-78341-3	book	January 2008
Principles of Terrestrial Ecosystem Ecology Chapin, F. Stuart; Matson, Pamela A.; Vitousek, Peter M. https://doi.org/10.1007/978-1-4419-9504-9	book	September 2011
The Diversity and Co-occurrence Patterns of N2-Fixing Communities in a CO2-Enriched Grassland Ecosystem Tu, Qichao; Zhou, Xishu; He, Zhili Microbial Ecology, Vol. 71, Issue 3 https://doi.org/10.1007/s00248-015-0659-7	journal	August 2015
Biological dinitrogen fixation and soil microbial biomass carbon as influenced by free-air carbon dioxide enrichment (FACE) at three levels of nitrogen fertilization in a paddy field Hoque, Mozammel; Inubushi, Kazuyuki; Miura, Shu Biology and Fertility of Soils, Vol. 34, Issue 6 https://doi.org/10.1007/s00374-001-0430-8	journal	December 2001
Elevated CO2, litter chemistry, and decomposition: a synthesis Norby, Richard J.; Cotrufo, M. Francesca; Ineson, Philip Oecologia, Vol. 127, Issue 2 https://doi.org/10.1007/s004420000615	journal	April 2001
Soil moisture dynamics of calcareous grassland under elevated CO 2 Niklaus, Pascal A.; Spinnler, D.; Körner, C. Oecologia, Vol. 117, Issue 1-2 https://doi.org/10.1007/s004420050649	journal	November 1998
Long-Term Leaf Production Response to Elevated Atmospheric Carbon Dioxide and Tropospheric Ozone Talhelm, Alan F.; Pregitzer, Kurt S.; Giardina, Christian P. Ecosystems, Vol. 15, Issue 1 https://doi.org/10.1007/s10021-011-9493-z	journal	November 2011
Nitrogen Cycles: Past, Present, and Future Galloway, J. N.; Dentener, F. J.; Capone, D. G. Biogeochemistry, Vol. 70, Issue 2 https://doi.org/10.1007/s10533-004-0370-0	journal	September 2004
N2O and NO emission from agricultural fields and soils under natural vegetation: summarizing available measurement data and modeling of global annual emissions Stehfest, Elke; Bouwman, Lex Nutrient Cycling in Agroecosystems, Vol. 74, Issue 3 https://doi.org/10.1007/s10705-006-9000-7	journal	March 2006
Nitrogen mineralization in density fractions of soil organic matter from maize and legume cropping systems Barrios, E.; Buresh, R. J.; Sprent, J. I. Soil Biology and Biochemistry, Vol. 28, Issue 10-11 https://doi.org/10.1016/S0038-0717(96)00155-1	journal	October 1996
Water use of a bioenergy plantation increases in a future high CO2 world Tricker, Penny J.; Pecchiari, Marco; Bunn, Steve M. Biomass and Bioenergy, Vol. 33, Issue 2 https://doi.org/10.1016/j.biombioe.2008.05.009	journal	February 2009
The effect of nitrogen form on rhizosphere soil pH and zinc phytoextraction by Thlaspi caerulescens Monsant, A. C.; Tang, C.; Baker, A. J. M. Chemosphere, Vol. 73, Issue 5 https://doi.org/10.1016/j.chemosphere.2008.07.034	journal	October 2008
Fungal/bacterial ratios in grasslands with contrasting nitrogen management de Vries, Franciska T.; Hoffland, Ellis; van Eekeren, Nick Soil Biology and Biochemistry, Vol. 38, Issue 8 https://doi.org/10.1016/j.soilbio.2006.01.008	journal	August 2006
Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique Rousk, Johannes; Bååth, Erland Soil Biology and Biochemistry, Vol. 39, Issue 8 https://doi.org/10.1016/j.soilbio.2007.03.023	journal	August 2007
Evaluation of nitrate and ammonium as sources of NO and N2O emissions from black earth soils (Haplic Chernozem) based on 15N field experiments Russow, R.; Spott, O.; Stange, C. F. Soil Biology and Biochemistry, Vol. 40, Issue 2 https://doi.org/10.1016/j.soilbio.2007.08.020	journal	February 2008
Impact of a low level of CO2 enrichment on soil carbon and nitrogen pools and mineralization rates over ten years in a seasonally dry, grazed pasture Ross, D. J.; Newton, P. C. D.; Tate, K. R. Soil Biology and Biochemistry, Vol. 58 https://doi.org/10.1016/j.soilbio.2012.12.011	journal	March 2013
Physical and biogeochemical controls over terrestrial ecosystem responses to nitrogen deposition Asner, Gregory P.; Townsend, Alan R.; Riley, William J. Biogeochemistry, Vol. 54, Issue 1, p. 1-39 https://doi.org/10.1023/A:1010653913530	journal	January 2001
Global patterns of terrestrial biological nitrogen (N ₂ ) fixation in natural ecosystems Cleveland, Cory C.; Townsend, Alan R.; Schimel, David S. Global Biogeochemical Cycles, Vol. 13, Issue 2 https://doi.org/10.1029/1999GB900014	journal	June 1999
Emissions of N ₂ O from tropical forest soils: Response to fertilization with NH ₄ ⁺ , NO ₃ ⁻ , and PO ₄ ³⁻ Keller, M.; Kaplan, W. A.; Wofsy, S. C. Journal of Geophysical Research, Vol. 93, Issue D2 https://doi.org/10.1029/JD093iD02p01600	journal	January 1988
Continuous CO2 enrichment leads to increased nodule biomass, carbon availability to nodules and activity of carbon-metabolising enzymes but does not enhance specific nitrogen fixation in pea Cabrerizo, Pablo M.; Gonzalez, Esther M.; Aparicio-Tejo, Pedro M. Physiologia Plantarum, Vol. 113, Issue 1 https://doi.org/10.1034/j.1399-3054.2001.1130105.x	journal	September 2001
Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere Oren, Ram; Ellsworth, David S.; Johnsen, Kurt H. Nature, Vol. 411, Issue 6836 https://doi.org/10.1038/35078064	journal	May 2001
Nitrogen limitation constrains sustainability of ecosystem response to CO2 Reich, Peter B.; Hobbie, Sarah E.; Lee, Tali Nature, Vol. 440, Issue 7086 https://doi.org/10.1038/nature04486	journal	April 2006
Increased soil emissions of potent greenhouse gases under increased atmospheric CO2 van Groenigen, Kees Jan; Osenberg, Craig W.; Hungate, Bruce A. Nature, Vol. 475, Issue 7355 https://doi.org/10.1038/nature10176	journal	July 2011
Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise Keenan, Trevor F.; Hollinger, David Y.; Bohrer, Gil Nature, Vol. 499, Issue 7458 https://doi.org/10.1038/nature12291	journal	July 2013
Key role of symbiotic dinitrogen fixation in tropical forest secondary succession Batterman, Sarah A.; Hedin, Lars O.; van Breugel, Michiel Nature, Vol. 502, Issue 7470 https://doi.org/10.1038/nature12525	journal	September 2013
Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass Reich, Peter B.; Hobbie, Sarah E. Nature Climate Change, Vol. 3, Issue 3 https://doi.org/10.1038/nclimate1694	journal	September 2012
Carbon benefits of anthropogenic reactive nitrogen offset by nitrous oxide emissions Zaehle, Sönke; Ciais, Philippe; Friend, Andrew D. Nature Geoscience, Vol. 4, Issue 9 https://doi.org/10.1038/ngeo1207	journal	July 2011
Global nitrogen deposition and carbon sinks Reay, Dave S.; Dentener, Frank; Smith, Pete Nature Geoscience, Vol. 1, Issue 7 https://doi.org/10.1038/ngeo230	journal	June 2008
Plant growth and competition at elevated CO2: on winners, losers and functional groups: Tansley review Poorter, Hendrik; Navas, Marie-Laure New Phytologist, Vol. 157, Issue 2 https://doi.org/10.1046/j.1469-8137.2003.00680.x	journal	January 2003
CO2 enhancement of forest productivity constrained by limited nitrogen availability Norby, R. J.; Warren, J. M.; Iversen, C. M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 45 https://doi.org/10.1073/pnas.1006463107	journal	October 2010
Effect of nitrogen fertilizer form on pH of the bulk soil and rhizosphere, and on the growth, phosphorus, and micronutrient uptake of bean Thomson, C. J.; Marschner, H.; Römheld, V. Journal of Plant Nutrition, Vol. 16, Issue 3 https://doi.org/10.1080/01904169309364548	journal	March 1993
Global patterns of the responses of leaf-level photosynthesis and respiration in terrestrial plants to experimental warming Liang, Junyi; Xia, Jianyang; Liu, Lingli Journal of Plant Ecology, Vol. 6, Issue 6 https://doi.org/10.1093/jpe/rtt003	journal	February 2013
Long-term response of a Mojave Desert winter annual plant community to a whole-ecosystem atmospheric CO ₂ manipulation (FACE) Smith, Stanley D.; Charlet, Therese N.; Zitzer, Stephen F. Global Change Biology, Vol. 20, Issue 3 https://doi.org/10.1111/gcb.12411	journal	January 2014
Ten years of free-air CO ₂ enrichment altered the mobilization of N from soil in Lolium perenne L. swards Schneider, Manuel K.; Lüscher, Andreas; Richter, Michael Global Change Biology, Vol. 10, Issue 8 https://doi.org/10.1111/j.1365-2486.2004.00803.x	journal	August 2004
Annual basal area increment and growth duration of Pinus taeda in response to eight years of free-air carbon dioxide enrichment Moore, David J. P.; Aref, Susanne; Ho, Ringo M. Global Change Biology, Vol. 12, Issue 8 https://doi.org/10.1111/j.1365-2486.2006.01189.x	journal	August 2006
Interactions between plant growth and soil nutrient cycling under elevated CO ₂ : a meta-analysis de GRAAFF, Marie-Anne; van GROENIGEN, Kees-Jan; Six, Johan Global Change Biology, Vol. 12, Issue 11 https://doi.org/10.1111/j.1365-2486.2006.01240.x	journal	November 2006
Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development McCarthy, Heather R.; Oren, Ram; Johnsen, Kurt H. New Phytologist, Vol. 185, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03078.x	journal	November 2009
Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems Iversen, Colleen M. New Phytologist, Vol. 186, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03122.x	journal	December 2009
Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis Lu, Meng; Yang, Yuanhe; Luo, Yiqi New Phytologist, Vol. 189, Issue 4 https://doi.org/10.1111/j.1469-8137.2010.03563.x	journal	December 2010
Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization Rousk, J.; Brookes, P. C.; Baath, E. Applied and Environmental Microbiology, Vol. 75, Issue 6 https://doi.org/10.1128/AEM.02775-08	journal	January 2009
Gas Exchange of Legume Nodules and the Regulation of Nitrogenase Activity Hunt, S.; Layzell, D. B. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 44, Issue 1 https://doi.org/10.1146/annurev.pp.44.060193.002411	journal	June 1993
Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide Luo, Yiqi; Su, Bo; Currie, William S. BioScience, Vol. 54, Issue 8 https://doi.org/10.1641/0006-3568(2004)054[0731:PNLOER]2.0.CO;2	journal	January 2004
The Meta-Analysis of Response Ratios in Experimental Ecology Hedges, Larry V.; Gurevitch, Jessica; Curtis, Peter S. Ecology, Vol. 80, Issue 4 https://doi.org/10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2	journal	June 1999
VALIDITY OF EXTRAPOLATING FIELD CO ₂ EXPERIMENTS TO PREDICT CARBON SEQUESTRATION IN NATURAL ECOSYSTEMS Luo, Yiqi; Reynolds, James F. Ecology, Vol. 80, Issue 5 https://doi.org/10.1890/0012-9658(1999)080[1568:VOEFCE]2.0.CO;2	journal	July 1999
Controls on Nitrogen Cycling in Terrestrial Ecosystems: a Synthetic Analysis of Literature data Booth, Mary S.; Stark, John M.; Rastetter, Edward Ecological Monographs, Vol. 75, Issue 2 https://doi.org/10.1890/04-0988	journal	May 2005
ELEVATED CO ₂ STIMULATES NET ACCUMULATIONS OF CARBON AND NITROGEN IN LAND ECOSYSTEMS: A META-ANALYSIS Luo, Yiqi; Hui, Dafeng; Zhang, Deqiang Ecology, Vol. 87, Issue 1 https://doi.org/10.1890/04-1724	journal	January 2006
PROGRESSIVE NITROGEN LIMITATION OF ECOSYSTEM PROCESSES UNDER ELEVATED CO ₂ IN A WARM-TEMPERATE FOREST Finzi, Adrien C.; Moore, David J. P.; DeLucia, Evan H. Ecology, Vol. 87, Issue 1 https://doi.org/10.1890/04-1748	journal	January 2006
RESPONSES OF N-LIMITED ECOSYSTEMS TO INCREASED CO ₂ : A BALANCED-NUTRITION, COUPLED-ELEMENT-CYCLES MODEL Rastetter, Edward B.; Ågren, Göran I.; Shaver, Gaius R. Ecological Applications, Vol. 7, Issue 2 https://doi.org/10.1890/1051-0761(1997)007[0444:RONLET]2.0.CO;2	journal	May 1997
Nitrogen Mineralization Responses to Cropping, Tillage, and Nitrogen Rate in the Northern Great Plains Wienhold, Brian J.; Halvorson, Ardell D. Soil Science Society of America Journal, Vol. 63, Issue 1 https://doi.org/10.2136/sssaj1999.03615995006300010027x	journal	January 1999

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