Constraints to nitrogen acquisition of terrestrial plants under elevated CO2
Corresponding Author
Zhaozhong Feng
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, P.O. Box 2871, 100085 Beijing, China
Correspondence: Zhaozhong Feng, tel. + 86 10 62943823, fax +86 10 62943822, e-mail: [email protected] and Dr Johan Uddling, tel. + 46 31 7866663, fax + 46 31 7862560, e-mail: [email protected]Search for more papers by this authorTobias Rütting
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
Department of Earth Sciences, University of Gothenburg, P.O. Box 460, 405 30 Gothenburg, Sweden
Search for more papers by this authorHåkan Pleijel
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
Search for more papers by this authorGöran Wallin
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
Search for more papers by this authorPeter B. Reich
Department of Forest Resources, University of Minnesota, 1530 Cleveland Avenue North, St. Paul, MN, 55108 USA
Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, NSW, 2753 Australia
Search for more papers by this authorClaudia I. Kammann
Department of Plant Ecology, Justus-Liebig-University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany
Search for more papers by this authorPaul C.D. Newton
AgResearch Grasslands, Private Bag 11008, Palmerston North, New Zealand
Search for more papers by this authorKazuhiko Kobayashi
Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 113-8657 Japan
Search for more papers by this authorYunjian Luo
Institute of Urban Environment, Chinese Academy of Sciences, 361021 Xiamen, China
Search for more papers by this authorJohan Uddling
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
Search for more papers by this authorCorresponding Author
Zhaozhong Feng
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, P.O. Box 2871, 100085 Beijing, China
Correspondence: Zhaozhong Feng, tel. + 86 10 62943823, fax +86 10 62943822, e-mail: [email protected] and Dr Johan Uddling, tel. + 46 31 7866663, fax + 46 31 7862560, e-mail: [email protected]Search for more papers by this authorTobias Rütting
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
Department of Earth Sciences, University of Gothenburg, P.O. Box 460, 405 30 Gothenburg, Sweden
Search for more papers by this authorHåkan Pleijel
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
Search for more papers by this authorGöran Wallin
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
Search for more papers by this authorPeter B. Reich
Department of Forest Resources, University of Minnesota, 1530 Cleveland Avenue North, St. Paul, MN, 55108 USA
Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, NSW, 2753 Australia
Search for more papers by this authorClaudia I. Kammann
Department of Plant Ecology, Justus-Liebig-University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany
Search for more papers by this authorPaul C.D. Newton
AgResearch Grasslands, Private Bag 11008, Palmerston North, New Zealand
Search for more papers by this authorKazuhiko Kobayashi
Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 113-8657 Japan
Search for more papers by this authorYunjian Luo
Institute of Urban Environment, Chinese Academy of Sciences, 361021 Xiamen, China
Search for more papers by this authorJohan Uddling
Department of Biological and Environmental Sciences, University of Gothenburg, P.O. Box 461, 405 30 Gothenburg, Sweden
Search for more papers by this authorAbstract
A key part of the uncertainty in terrestrial feedbacks on climate change is related to how and to what extent nitrogen (N) availability constrains the stimulation of terrestrial productivity by elevated CO2 (eCO2), and whether or not this constraint will become stronger over time. We explored the ecosystem-scale relationship between responses of plant productivity and N acquisition to eCO2 in free-air CO2 enrichment (FACE) experiments in grassland, cropland and forest ecosystems and found that: (i) in all three ecosystem types, this relationship was positive, linear and strong (r2 = 0.68), but exhibited a negative intercept such that plant N acquisition was decreased by 10% when eCO2 caused neutral or modest changes in productivity. As the ecosystems were markedly N limited, plants with minimal productivity responses to eCO2 likely acquired less N than ambient CO2-grown counterparts because access was decreased, and not because demand was lower. (ii) Plant N concentration was lower under eCO2, and this decrease was independent of the presence or magnitude of eCO2-induced productivity enhancement, refuting the long-held hypothesis that this effect results from growth dilution. (iii) Effects of eCO2 on productivity and N acquisition did not diminish over time, while the typical eCO2-induced decrease in plant N concentration did. Our results suggest that, at the decennial timescale covered by FACE studies, N limitation of eCO2-induced terrestrial productivity enhancement is associated with negative effects of eCO2 on plant N acquisition rather than with growth dilution of plant N or processes leading to progressive N limitation.
Supporting Information
| Filename | Description |
|---|---|
| gcb12938-sup-0001-TableS1-FigS1-S3.docxWord document, 43.1 KB | Table S1. Aboveground litter N concentration (%) across species, N levels and experimental years at each FACE site. Fig. S1. Effect of elevated CO2 on the N concentration ([N]) of the annual production of above- and belowground plant parts. Fig. S2. Effect of elevated CO2 (eCO2) on (a) whole-plant net primary production (NPP) and (b) corresponding nitrogen acquisition (Nac) in relation to the number of years of experimental CO2 exposure at each FACE site. Fig. S3. Effect of elevated CO2 (eCO2) on (a) aboveground net primary production (ANPP) and (b) corresponding nitrogen acquisition (Nac) in relation to the number of years of experimental CO2 exposure in grassland ecosystems with low diversity and high diversity. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Adamsen FJ, Wechsung G, Wechsung F et al. (2005) Temporal changes in soil and biomass nitrogen for irrigated wheat grown under free-air carbon dioxide enrichment (FACE). Agronomy Journal, 97, 160–168.
- Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytologist, 165, 351–371.
- Ballantyne AP, Alden CB, Miller JB, Tans PP, White JWC (2012) Increase in observed net carbon dioxide uptake by land and oceans during the past 50 years. Nature, 488, 70–72.
- Bloom AJ, Burger M, Rubio-Asensio JS, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science, 328, 899–903.
- Bloom AJ, Rubio-Asensio JS, Randall L, Rachmilevitch S, Cousins AB, Carlisle EA (2012) CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology, 93, 355–367.
- Bloom AJ, Burger M, Kimball BA, Pinter PJJ (2014) Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nature Climate Change, 4, 477–480.
- Cheng L, Booker FL, Tu C et al. (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science, 337, 1084–1087.
- Comins HN, McMurtrie RE (1993) Long-term response of nutrient-limited forests to CO”2 enrichment; Equilibrium behavior of plant-soil models. Ecological Applications, 3, 666–681.
- Curtis PS (1996) A meta-analysis of leaf gas exchange and nitrogen in trees grown under elevated carbon dioxide. Plant Cell and Environment, 19, 127–137.
- Diaz S, Grime JP, Harris J, McPherson E (1993) Evidence of a feedback mechanism limiting plant-response to elevated carbon dioxide. Nature, 364, 616–617.
- Dijkstra FA, Pendall E, Mosier AR, King JY, Milchunas DG, Morgan JA (2008) Long-term enhancement of N availability and plant growth under elevated CO2 in a semi-arid grassland. Functional Ecology, 22, 975–982.
- Dong GC, Wang YL, Yang HJ et al. (2002) Effect of free-air CO2 enrichment (FACE) on nitrogen accumulation and utilization efficiency in rice (Oryza sativa). Chinese Journal of Applied Ecology, 13, 1219–1222. (in Chinese).
- Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Global Change Biology, 10, 2121–2138.
- Esmeijer-Liu AJ, Aerts R, Kuerschner WM, Bobbink R, Lotter AF, Verhoeven JTA (2009) Nitrogen enrichment lowers Betula pendula green and yellow leaf stoichiometry irrespective of effects of elevated carbon dioxide. Plant and Soil, 316, 311–322.
- Falster DS, Warton DI, Wright IJ (2006) SMATR: Standardised Major Axis Tests and Routines, ver 2.0. Available at: http://www.bio.mq.edu.au/ecology/SMATR/.
- Finzi AC, Allen AS, DeLucia EH, Ellsworth DS, Schlesinger WH (2001) Forest litter production, chemistry, and decomposition following two years of free-air CO2 enrichment. Ecology, 82, 470–484.
- Finzi AC, Norby RJ, Calfapietra C et al. (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proceedings of the National Academy of Sciences, USA, 104, 14014–14019.
- Gifford RM, Barrett DJ, Lutze JL (2000) The effects of elevated CO2 on the C: N and C: P mass ratios of plant tissues. Plant and Soil, 224, 1–14.
- Gloser V, Jezikova M, Luscher A et al. (2000) Soil mineral nitrogen availability was unaffected by elevated atmospheric pCO2 in a four year old field experiment (Swiss FACE). Plant and Soil, 227, 291–299.
- de Graaff MA, van Groenigen KJ, Six J, Hungate B, van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Global Change Biology, 12, 2077–2091.
- Gross K, Cardinale BJ, Fox JW et al. (2014) Species richness and the temporal stability of biomass production: a new analysis of recent biodiversity experiments. American Naturalist, 183, 1–12.
- Grüters U, Janze S, Kammann C, Jäger HJ (2006) Plant functional types and elevated CO2: a method of scanning for causes of community alteration. Journal of Applied Botany and Food Quality-Angewandte Botanik, 80, 116–128.
- Hebeisen T, Luscher A, Zanetti S et al. (1997) Growth response of Trifolium repens L and Lolium perenne L as monocultures and bi-species mixture to free air CO2 enrichment and management. Global Change Biology, 3, 149–160.
- Hu SJ, Tu C, Chen X, Gruver JB (2006) Progressive N limitation of plant response to elevated CO2: a microbiological perspective. Plant and Soil, 289, 47–58.
- Huang JY, Yang HJ, Yang LX et al. (2004) Effects of free-air CO2 enrichment (FACE) on yield formation of rice (Oryza sativa L.) and its interaction with nitrogen. Scientia Agricultura Sinica, 37, 1824–1830. (in Chinese).
- Hungate BA, Dukes JS, Shaw MR, Luo Y, Field CB (2003) Nitrogen and climate change. Science, 302, 1512–1513.
- Hungate BA, Stiling PD, Dijkstra P et al. (2004) CO2 elicits long-term decline in nitrogen fixation. Science, 304, 1291.
- IPCC (2013) Climate Change 2013: The Physical Science Basis: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds TF Stocker, D Qin, GK Plattner, M Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex, PM Midgley), pp. 465–470. Cambridge University Press, Cambridge.
- Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytologist, 186, 346–357.
- Kammann C, Grunhage L, Gruters U, Janze S, Jager HJ (2005) Response of aboveground grassland biomass and soil moisture to moderate long-term CO2 enrichment. Basic and Applied Ecology, 6, 351–365.
- Kim HY, Lieffering M, Miura S, Kobayashi K, Okada M (2001) Growth and nitrogen uptake of CO2-enriched rice under field conditions. New Phytologist, 150, 223–229.
- Kim HY, Lieffering M, Kobayashi K, Okada M, Miura S (2003) Seasonal changes in the effects of elevated CO2 on rice at three levels of nitrogen supply: a free air CO2 enrichment (FACE) experiment. Global Change Biology, 9, 826–837.
- Ko J, Ahuja L, Kimball B et al. (2010) Simulation of free air CO2 enriched wheat growth and interactions with water, nitrogen, and temperature. Agricultural and Forest Meteorology, 150, 1331–1346.
- Kongstad J, Schmidt IK, Riis-Nielsen T, Arndal MF, Mikkelsen TN, Beier C (2012) High resilience in heathland plants to changes in temperature, drought, and CO2 in Combination: results from the CLIMAITE experiment. Ecosystems, 15, 269–283.
- Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytologist, 172, 393–411.
- Kuzyakov Y (2002) Review: Factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science, 165, 382–396.
- Larsen KS, Andresen LC, Beier C et al. (2011) Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments. Global Change Biology, 17, 1884–1899.
- Le Quere C, Raupach MR, Canadell JG et al. (2009) Trends in the sources and sinks of carbon dioxide. Nature Geoscience, 2, 831–836.
- Le Quere C, Andres RJ, Boden T et al. (2013) The global carbon budget 1959–2011. Earth System Science Data, 5, 165–185.
- Lee TD, Barrott SH, Reich PB (2011) Photosynthetic responses of 13 grassland species across 11 years of free-air CO2 enrichment is modest, consistent and independent of N supply. Global Change Biology, 17, 2893–2904.
- Leuzinger S, Luo YQ, Beier C, Dieleman W, Vicca S, Korner C (2011) Do global change experiments overestimate impacts on terrestrial ecosystems? Trends in Ecology and Evolution, 26, 236–241.
- Li FY, Newton PCD, Lieffering M (2014) Testing simulations of intra- and inter-annual variation in the plant production response to elevated CO2 against measurements from an 11-year FACE experiment on grazed pasture. Global Change Biology, 20, 228–239.
- Lindroth RL, Kopper BJ, Parsons WFJ et al. (2001) Consequences of elevated carbons dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). Environmental Pollution, 115, 395–404.
- Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends in Ecology and Evolution, 17, 457–461.
- Long SP, Drake BG (1992) Photosynthetic CO2 assimilation and rising atmospheric CO2 concentrations. In: Crop Photosynthesis: Spacial and Temporal Determinant (eds NR Baker, H Thomas), pp. 69–103. Elsevier Sci, Amsterdam.
10.1016/B978-0-444-89608-7.50011-3 Google Scholar
- Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annual Review of Plant Biology, 55, 591–628.
- Luo YQ, Su B, Currie WS et al. (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience, 54, 731–739.
- Luo YQ, Hui DF, Zhang DQ (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology, 87, 53–63.
- McCarthy HR, Oren R, Johnsen KH et al. (2010) 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. New Phytologist, 185, 514–528.
- McDonald EP, Erickson JE, Kruger EL (2002) Can decreased transpiration limit plant nitrogen acquisition in elevated CO2? Functional Plant Biology, 29, 1115–1120.
- McGrath JM, Lobell DB (2013) Reduction of transpiration and altered nutrient allocation contribute to nutrient decline of crops grown in elevated CO2 concentrations. Plant Cell and Environment, 36, 697–705.
- McMurtrie RE, Norby RJ, Medlyn BE et al. (2008) Why is plant-growth response to elevated CO2 amplified when water is limiting, but reduced when nitrogen is limiting? A growth-optimisation hypothesis. Functional Plant Biology, 35, 521–534.
- Myers SS, Zanobetti A, Kloog I et al. (2014) Increasing CO2 threatens human nutrition. Nature, 510, 139–142.
- Newton PCD, Lieffering M, Bowatte W et al. (2010) The rate of progression and stability of progressive nitrogen limitation at elevated atmospheric CO2 in a grazed grassland over 11 years of Free Air CO2 enrichment. Plant and Soil, 336, 433–441.
- Newton PCD, Lieffering M, Parsons AJ et al. (2014) Selective grazing modifies previously anticipated responses of plant community composition to elevated CO2 in temperate grassland. Global Change Biology, 20, 158–169.
- Norby RJ (2009) Carbon Dioxide Information Analysis Center (http://cdiac.ornl.gov), U.S. Department of Energy, Oak Ridge National Laboratory, Oak Ridge, TN.
- Norby RJ, Iversen CM (2006) Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. Ecology, 87, 5–14.
- Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell and Environment, 22, 683–714.
- Norby RJ, Cotrufo MF, Ineson P, O'Neill EG, Canadell JG (2001) Elevated CO2, litter chemistry, and decomposition: a synthesis. Oecologia, 127, 153–165.
- Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proceedings of the National Academy of Sciences, USA, 107, 19368–19373.
- Oren R, Ellsworth DS, Johnsen KH et al. (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature, 411, 469–472.
- Parton WJ, Hanson PJ, Swanston C, Torn M, Trumbore WR, Riley W, Kelly R (2010) ForCent model development and testing using the enriched background isotope study experiment. Journal of Geophysical Research: Biogeosciences, 115, G04001.
- 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. Ecology Letters, 14, 187–194.
- Pleijel H, Uddling J (2012) Yield vs. quality trade-offs for wheat in response to carbon dioxide and ozone. Global Change Biology, 18, 596–605.
- Poorter H, VanBerkel Y, Baxter R et al. (1997) The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species. Plant Cell Environment, 20, 472–482.
- Rastetter EB, McKane RB, Shaver GR, Melillo JM (1992) Changes in C-storages by terrestrial ecosystems – How C-N interactions restrict responses to CO2 and temperature. Water Air and Soil Pollution, 64, 327–344.
- Reich PB (2009) BioCON: Biodiversity, Elevated CO2, and N Enrichment -Experiment 141. Available at: http://www.cedarcreek.umn.edu/research/data/index.php.
- Reich PB, Hobbie SE (2013) Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nature Climate Change, 3, 278–282.
- Reich PB, Tilman D, Craine J et al. (2001) Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? A field test with 16 grassland species. New Phytologist, 150, 435–448.
- Reich PB, Tilman D, Naeem S et al. (2004) Species and functional group diversity independently influence biomass accumulation and its response to CO2 and N. Proceedings of the National Academy of Sciences, USA, 101, 10101–10106.
- Reich PB, Hobbie SE, Lee T et al. (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature, 440, 922–925.
- Reich PB, Tilman D, Isbell F et al. (2012) Impacts of biodiversity loss escalate through time as redundancy fades. Science, 336, 589–592.
- Rosenberg MS, Gurevitch J, Adams DC (2000) MetaWin: Statistical Software for Meta-Analysis: Version 2.1. Sinauer Associates, Inc., Sunderland, Massachusetts.
- Ross DJ, Newton PCD, Tate KR (2004) Elevated [CO2] effects on herbage production and soil carbon and nitrogen pools and mineralization in a species-rich, grazed pasture on a seasonally dry sand. Plant and Soil, 260, 183–196.
- Rütting T, Andresen LC (2015) Nitrogen cycle responses to elevated CO2 depend on ecosystem nutrient status. Nutrient Cycling in Agroecosystems, 101, 285–294.
- Rütting T, Clough TJ, Mueller C, Lieffering M, Newton PCD (2010) Ten years of elevated atmospheric carbon dioxide alters soil nitrogen transformations in a sheep-grazed pasture. Global Change Biology, 16, 2530–2542.
- Schneider MK, Luscher A, Richter M et al. (2004) Ten years of free-air CO2 enrichment altered the mobilization of N from soil in Lolium perenne L. swards. Global Change Biology, 10, 1377–1388.
- Shimono H, Okada M, Yamakawa Y, Nakamura H, Kobayashi K, Hasegawa T (2008) Rice yield enhancement by elevated CO2 is reduced in cool weather. Global Change Biology, 14, 276–284.
- Shimono H, Okada M, Yamakawa Y, Nakamura H, Kobayashi K, Hasegawa T (2009) Genotypic variation in rice yield enhancement by elevated CO2 relates to growth before heading, and not to maturity group. Journal of Experimental Botany, 60, 523–532.
- Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell and Environment, 22, 583–621.
- Strain BR, Bazzaz FA (1983) Terrestrial plant communities. In: CO2 and Plants (ed. ER Lemon), pp. 177–222. Westview, Boulder, Colo.
- Talhelm AF, Pregitzer KS, Kubiske ME et al. (2014) Elevated carbon dioxide and ozone alter productivity and ecosystem carbon content in northern temperate forests. Global Change Biology, 20, 2492–2504.
- Taub DR, Wang X (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. Journal of Integrative Plant Biology, 50, 1365–1374.
- Watanabe T, Bowatte S, Newton PCD (2013) A reduced fraction of plant N derived from atmospheric N (%Ndfa) and reduced rhizobial nifH gene numbers indicate a lower capacity for nitrogen fixation in nodules of white clover exposed to long-term CO2 enrichment. Biogeosciences, 10, 8269–8281.
- Weigel H-J, Manderscheid R (2012) Crop growth responses to free air CO2 enrichment and nitrogen fertilization: rotating barley, ryegrass, sugar beet and wheat. European Journal of Agronomy, 43, 97–107.
- Yang LX, Huang JY, Yang HJ et al. (2006) Seasonal changes in the effects of free-air CO2 enrichment (FACE) on dry matter production and distribution of rice (Oryza sativa L.). Field Crops Research, 98, 12–19.
- Yang L, Huang J, Yang H et al. (2007a) Seasonal changes in the effects of free-air CO2 enrichment (FACE) on nitrogen (N) uptake and utilization of rice at three levels of N fertilization. Field Crops Research, 100, 189–199.
- Yang LX, Huang JY, Li SF et al. (2007b) Effects of free-air CO2 enrichment on nitrogen uptake and utilization of wheat. Chinese Journal of Applied Ecology, 18, 519–525. (In Chinese).
- Yang LX, Wang YL, Li SF et al. (2007c) Effects of free-air CO2 enrichment (FACE) on dry matter production and allocation in wheat. Chinese Journal of Applied Ecology, 18, 339–346. (In Chinese).
- Yang LX, Liu HJ, Wang YX et al. (2009) Impact of elevated CO2 concentration on inter-subspecific hybrid rice cultivar Liangyoupeijiu under fully open-air field conditions. Field Crops Research, 112, 7–15.
- Zaehle S, Medlyn BE, De Kauwe MG et al. (2014) Evaluation of 11 terrestrial carbon-nitrogen cycle models against observations from two temperate free-Air CO2 enrichment studies. New Phytologist, 202, 803–822.
- Zak DR, Pregitzer KS, Curtis PS, Teeri JA, Fogel R, Randlett DL (1993) Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant and Soil, 151, 105–117.
- Zanetti S, Hartwig UA, vanKessel C et al. (1997) Does nitrogen nutrition restrict the CO2 response of fertile grassland lacking legumes? Oecologia, 112, 17–25.
