Skip to main content

RETRACTED ARTICLE: CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: a meta-analysis

Plant Ecology volume 213, pages 505–521 (2012)Cite this article

This article was retracted on 18 November 2015

Abstract

Elevated CO2 is expected to lower plant nutrient concentrations via carbohydrate dilution and increased nutrient use efficiency. Elevated CO2 consistently lowers plant foliar nitrogen, but there is no consensus on CO2 effects across the range of plant nutrients. We used meta-analysis to quantify elevated CO2 effects on leaf, stem, root, and seed concentrations of B, Ca, Cu, Fe, K, Mg, Mn, P, S, and Zn among four plant functional groups and two levels of N fertilization. CO2 effects on plant nutrient concentration depended on the nutrient, plant group, tissue, and N status. CO2 reduced B, Cu, Fe, and Mg, but increased Mn concentration in the leaves of N2 fixers. Elevated CO2 increased Cu, Fe, and Zn, but lowered Mn concentration in grass leaves. Tree leaf responses were strongly related to N status: CO2 significantly decreased Cu, Fe, Mg, and S at high N, but only Fe at low N. Elevated CO2 decreased Mg and Zn in crop leaves grown with high N, and Mn at low N. Nutrient concentrations in crop roots were not affected by CO2 enrichment, but CO2 decreased Ca, K, Mg and P in tree roots. Crop seeds had lower S under elevated CO2. We also tested the validity of a “dilution model.” CO2 reduced the concentration of plant nutrients 6.6% across nutrients and plant groups, but the reduction is less than expected (18.4%) from carbohydrate accumulation alone. We found that elevated CO2 impacts plant nutrient status differently among the nutrient elements, plant functional groups, and among plant tissues. Our synthesis suggests that differences between plant groups and plant organs, N status, and differences in nutrient chemistry in soils preclude a universal hypothesis strictly related to carbohydrate dilution regarding plant nutrient response to elevated CO2.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. Springer, New York

    Book  Google Scholar 

  • Almeida JPF, Luscher A, Frehner M, Oberson A, Nösberger J (1999) Partitioning of P and the activity of root acid phosphatase in white clover (Trifolium repens L.) are modified by increased atmospheric CO2 and P fertilization. Plant Soil 210:159–166

    CAS  Article  Google Scholar 

  • Barnes JD, Pfirrmann T (1992) The influence of CO2 and O3, singly and in combination, on gas exchange, growth and nutrient status of radish (Raphanus sativus). New Phytol 121:403–412

    CAS  Article  Google Scholar 

  • Baxter R, Gantley M, Ashenden TW, Farrar JF (1994) Effects of elevated carbon dioxide on three grass species from montane pasture. II. Nutrient uptake, allocation and efficiency of use. J Exp Bot 45:1267–1278

    CAS  Article  Google Scholar 

  • Baxter R, Ashenden TW, Farrar JF (1997) Effect of elevated CO2 and nutrient status on growth, dry matter partitioning and nutrient content of Poa alpina var. vivipara L. J Exp Bot 48:1477–1486

    CAS  Article  Google Scholar 

  • Bazzaz FA (1990) The response of natural ecosystems to the rising global CO2 levels. Annu Rev Ecol Syst 21:167–196

    Article  Google Scholar 

  • Blank RR, Derner JD (2004) Effects of CO2 enrichment on plant-soil relationships of Lepidium latifolium. Plant Soil 262:159–167

    CAS  Article  Google Scholar 

  • Blank RR, White RH, Ziska LH (2006) Combustion properties of Bromus tectorum L.: influence of ecotype and growth under four CO2 concentrations. Int J Wildland Fire 15:227–236

    CAS  Article  Google Scholar 

  • Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903

    CAS  PubMed  Article  Google Scholar 

  • Brady NC, Weil RR (2002) The nature and properties of soils. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Campbell CD, Sage RF (2002) Effects of CO2 and P on proteoid root formation in white lupin (Lupinus albus). Plant Cell Environ 25:1051–1059

    Article  Google Scholar 

  • Cao W, Tibbitts TW (1997) Starch concentration and impact on specific leaf weight and element concentrations in potato leaves under varied carbon dioxide and temperature. J Plant Nutr 20:871–881

    CAS  PubMed  Article  Google Scholar 

  • Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. PNAS 104:4990–4995

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Cheng W, Johnson DW (1998) Elevated CO2, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202:167–174

    CAS  Article  Google Scholar 

  • Cheng W, Sakai H, Yagi K, Hasegawa (2009) Interactions of elevated CO2 and night temperature on rice growth and yield. Agric For Meteorol 149:51–58

  • Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Glob Change Biol 4:43–54

    Article  Google Scholar 

  • de Graaff MA, van Groenigen KJ, Six J, Hungate BA, Van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Change Biol 12:2077–2091

    Article  Google Scholar 

  • De la Puente LS, Perez PP, Martinez-Carrasco R, Morcuende RM, Del Molino IMM (2000) Action of elevated CO2 and high temperatures on the mineral chemical composition of two varieties of wheat. Agrochimica 44:221–230

    Google Scholar 

  • Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639

    CAS  PubMed  Article  Google Scholar 

  • Duval BD, Dijkstra P, Natali SM, Megonigal JP, Ketterer ME, Lerdau MT, Gordon G, Anbar A, Hungate BA (2011) Plant-soil distribution of potentially toxic elements in response to elevated CO2. Environ Sci Technol 45:2570–2574

    CAS  PubMed  Article  Google Scholar 

  • Ebersberger D, Niklaus PA, Kandeler E (2003) Long term CO2 enrichment stimulates N-mineralization and enzyme activities in calcareous grassland. Soil Biol Biochem 35:965–972

    CAS  Article  Google Scholar 

  • Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Fangmeier A, Grüters U, Högy P, Vermehren B, Jäger HJ (1997) Effects of elevated CO2, nitrogen supply and tropospheric ozone on spring wheat II. Nutrients (N, P, K, S, Ca, Mg, Fe, Mn, Zn). Environ Pollut 96:43–59

    CAS  PubMed  Article  Google Scholar 

  • Fangmeier A, De Temmerman L, Mortensen L, Kemp K, Burke J, Mitchell R, van Oijen M, Weigel HJ (1999) Effects on nutrients and on grain quality in spring wheat crops grown under elevated CO2 concentrations and stress conditions in the European, multiple-site experiment ‘ESPACE-wheat’. Eur J Agron 10:215–229

    Article  Google Scholar 

  • Fangmeier A, De Temmerman L, Black C, Persson K, Vorne V (2002) Effects of elevated CO2 and/or ozone on nutrient concentrations and nutrient uptake of potatoes. Euro J Agron 17:353–368

    CAS  Article  Google Scholar 

  • Farrar JF, Jones DL (2000) The control of carbon acquisition by roots. New Phytol 147:43–53

    CAS  Article  Google Scholar 

  • 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

    Google Scholar 

  • 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. PNAS 104:14014–14019

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Fuhrer J (2003) Agroecosystem responses to combinations of elevated CO2, ozone, and global climate change. Agric Ecosyst Environ 97:1–20

    CAS  Article  Google Scholar 

  • Geissler N, Hussin S, Koyro H-W (2009) Elevated atmospheric CO2 concentration ameliorates effects of NaCl salinity on photosynthesis and leaf structure of Aster tripolium L. J Experiment Bot 60:137–151

    Google Scholar 

  • Goldberg S, Forster HS, Godfrey CL (1996) Molybdenum adsorption on oxides, clay minerals and soils. SSSAJ 60:425–432

    CAS  Article  Google Scholar 

  • Haase S, Rothe A, Kania A, Wasaki J, Romheld V, Engels C, Kandeler E, Neumann G (2008) Responses to iron limitation in Hordeum vulgare L. as affected by the atmospheric CO2 concentration. JEQ 37:1254–1262

    CAS  PubMed  Article  Google Scholar 

  • Heagle AS, Miller JE, Sherrill DE, Rawlings JO (1993) Effects of ozone and carbon dioxide mixtures on two clones of white clover. New Phytol 123:751–762

    CAS  Article  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Högy P, Fangmeier A (2008) Effects of elevated atmospheric CO2 on grain quality of wheat. J Cereal Sci 48:580–591. doi:10.1016/j.jcs.2008.01.006

    Article  CAS  Google Scholar 

  • Högy P, Fangmeier A (2009) Atmospheric CO2 enrichment affects potatoes: 2. Tuber quality traits. Eur J Agron 30:85–94

    Article  CAS  Google Scholar 

  • Huluka G, Hileman DR, Biswas PK, Lewin KF, Nagy J, Hendrey GR (1994) Effects of elevated CO2 and water stress on mineral concentration of cotton. Agric For Meteorol 70:141–152

    Article  Google Scholar 

  • Hungate BA, Dijkstra P, Johnson DW, Hinkle CR, Drake BG (1999) Elevated CO2 increases nitrogen fixation and decreases soil nitrogen mineralization in Florida scrub oak. Glob Change Biol 5:1–9

    Article  Google Scholar 

  • Hungate BA, Naiman RJ, Apps M, Cole JJ, Moldan B, Satake K, Stewart JWB, Victoria R, Vitousek PM (2003) Disturbance and element interactions. In: Melillo JM, Field CB, Moldan B (eds) Interactions of the major biogeochemical cycles, SCOPE 61. Island Press, Washington, pp 47–62

    Google Scholar 

  • Hungate BA, Stilling PD, Dijkstra P, Johnson DW, Ketterer ME, Hymus GJ, Hinkle CR, Drake BG (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304:1291

    CAS  PubMed  Article  Google Scholar 

  • Hunt R, Hand DW, Hannah MA, Neal AM (1995) Temporal and nutritional influences on the response to elevated CO2 in selected British grasses. Ann Bot 75:207–216

    Article  Google Scholar 

  • Intergovernmental Panel on Climate Change (2007) 4th assessment synthesis report, AR4. Valencia, Spain

    Google Scholar 

  • Jain V, Pal M, Raj A, Khetarapal S (2007) Photosynthesis and nutrient composition of spinach and fenugreek grown under elevated carbon dioxide concentration. Biol Plant 51:559–562

    CAS  Article  Google Scholar 

  • Jenny H (1980) The Soil Resource. Ecological Studies, vol 37. Springer-Verlag, New York, USA

    Book  Google Scholar 

  • Johnson DW, Hungate BA, Dijkstra P, Hymus GJ, Hinkle CR, Stiling P, Drake BG (2003) The effects of elevated CO2 on nutrient distribution in a fire-adapted scrub oak forest. Ecol Appl 13:1388–1399

    Article  Google Scholar 

  • Johnson DW, Cheng W, Joslin JD, Norby RJ, Edwards NT, Todd DE (2004) Effects of elevated CO2 on nutrient cycling in a sweetgum plantation. Biogeochemistry 69:379–403

    CAS  Article  Google Scholar 

  • Kabata-Pendias A (2001) Trace elements in soils and plants. CRC Press, Boca Raton, FL, USA

    Google Scholar 

  • Keutgen N, Chen K (2001) Responses of citrus leaf photosynthesis, chlorophyll fluorescence, macronutrient and carbohydrate contents to elevated CO2. J Plant Physiol 158:1307–1316

    CAS  Article  Google Scholar 

  • Knecht GN, O’Leary JW (1983) The influence of carbon dioxide on the growth, pigment, protein, carbocarbohydrate, and mineral status of lettuce. J Plant Nutr 6:301–312

    CAS  Article  Google Scholar 

  • Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540

    CAS  PubMed  Article  Google Scholar 

  • Langley JA, McKinley DC, Wolf AA, Hungate BA, Drake BG, Megonigal JP (2009) Priming depletes soil carbon and releases nitrogen in a scrub-oak ecosystem exposed to elevated CO2. Soil Biol Biochem 41:54–60

    CAS  Article  Google Scholar 

  • Le Thiec D, Dixon M, Loosveldt P, Garrec JP (1995) Seasonal and annual variations of phosphorus, calcium, potassium and manganese contents in different cross sections of Picea abies (L.) Karst. needles and Quercus rubra L. leaves exposed to elevated CO2. Trees 10:55–62

    Google Scholar 

  • Li Z, Tang S, Deng X, Wang R, Song Z (2010) Contrasting effects of elevated CO2 on Cu and Cd uptake by different rice varieties grown on contaminated soils with 2 levels of metals: implications for phytoextraction and food safety. J Hazard Mater 177:352–361

    Google Scholar 

  • Li J, Zhou JM, Duan ZQ, Du CW, Wang HY (2007) Effect of CO2 enrichment on the growth and nutrient uptake of tomato seedlings. Pedosphere 17:343–351

    CAS  Article  Google Scholar 

  • Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? TREE 17:457–461

    Google Scholar 

  • Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate BA, McMurtrie RE, Oren R, Parton WJ et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience 54:731–739

    Article  Google Scholar 

  • Luomala EM, Laittinem K, Suttinem S, Kellomaki S, Vavaavouri E (2005) Stomatal density, anatomy and nutrient concentrations of Scots pine needles are affected by elevated CO2 and temperature. Plant Cell Environ 28:733–749

    Google Scholar 

  • Lynch JP, Brown KM (2001) Topsoil foraging: an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237

    Google Scholar 

  • Ma H, Zhu J, Xie Z, Liu G, Zeng Q, Han Y (2007) Responses of rice and winter wheat to free-air CO2 enrichment (China FACE) at rice/wheat rotation system. Plant Soil 294:137–146. doi:10.1007/s11104-007-9241-5

    CAS  Article  Google Scholar 

  • Manderscheid R, Bender J, Jäger HJ, Weigel HJ (1995) Effects of season long CO2 enrichment on cereals. II. Nutrient concentrations and grain quality. Agric Ecosyst Environ 54:175–185

    CAS  Article  Google Scholar 

  • Melillo JM, Field CB, Moldan B (2003) Element interactions and the cycles of life: an overview. In: Melillo JM, Field CB, Moldan B (eds) Interactions of the major biogeochemical cycles: global change and human impacts. Interactions of the major biogeochemical cycles, SCOPE 61. Island Press, Washington, pp 1–12

    Google Scholar 

  • Morgan JA, Knight WG, Dudley LM, Hunt HW (1994) Enhanced root system C-sink activity, water relations and aspects of nutrient acquisition in mycotrophic Bouteloua gracilis subjected to CO2 enrichment. Plant Soil 165:139–146

    CAS  Article  Google Scholar 

  • Natali SM, Sanudo-Wilhelmy SA, Lerdau MT (2009) Plant and soil mediation of elevated CO2 impacts on trace metals. Ecosystems 12:715–727. doi:10.1007/s10021-009-9251-7

    CAS  Article  Google Scholar 

  • Newbery RM, Wolfenden J, Mansfield TA, Harrison AF (1995) Nitrogen, phosphorus and potassium uptake and demand in Agrostis capillaris: the influence of elevated CO2 and nutrient supply. New Phytol 130:565–574

    Article  Google Scholar 

  • Niinemets U, Tenhunen JD, Canta R, Chaves MM, Faria T, Pereira JS, Reynolds JF (1999) Interactive effects of nitrogen and phosphorus on the acclimation potential of foliage photosynthetic properties of cork oak, Quercus suber, to elevated atmospheric CO2 concentrations. Glob Change Biol 5:455–470

    Article  Google Scholar 

  • Norby RJ, O’Neill EG, Luxmoore RJ (1986) Effects of atmospheric CO2 enrichment on the growth and mineral nutrition of Quercus alba seedlings in nutrient poor soil. Plant Physiol 82:83–89

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, King JS, Ledford J, McCarthy HR, Moore DJP, Ceulemans R et al (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. PNAS 102:18052–18056

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • O’Neill EG, Luxmoore RJ, Norby RJ (1987) Elevated atmospheric CO2 effects on seedling growth, nutrient uptake, and rhizosphere bacterial populations of Liriodendron tulipifera L. I. Plant Soil 104:3–11

    Article  Google Scholar 

  • Oh N-W, Richter DD (2004) Soil acidification induced by elevated atmospheric CO2. Glob Change Biol 10:1936–1946

    Article  Google Scholar 

  • Oksanen E, Riikonen J, Kaakinen S, Holopainen T, Vapaavuori E (2005) Structural characteristics and chemical composition of birch (Betula pendula) leaves are modified by increasing CO2 and ozone. Glob Change Biol 11:732–748. doi:10.1111/j.1365-2486.2005.00938.x

    Article  Google Scholar 

  • Overdieck D (1993) Elevated CO2 and the mineral content of herbaceous and woody plants. Vegetatio 104:403–411

    Article  Google Scholar 

  • Pal M, Rao LS, Srivastava AC, Jain V, Sengupta UK (2003) Impact of CO2 enrichment and variable nitrogen supplies on composition and partitioning of essential nutrients of wheat. Biol Plant 47:227–231

    CAS  Article  Google Scholar 

  • Pal M, Karthikeyapandian V, Jain V, Srivastava AC, Raj A, Sengupta UK (2004) Biomass production and nutritional levels of berseem (Trifolium alexandrinum) grown under elevated CO2. Agric Ecosyst Environ 101:31–38

    Article  Google Scholar 

  • Peet MM, Huber SC, Patterson DT (1986) Acclimation to high CO2 in monoecious cucumbers II. Carbon exchange rates, enzyme activities, and starch and nutrient concentrations. Plant Physiol 80:63–67

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Peñuelas J, Idso SB, Ribas A, Kimball B (1997) Effects of long-term atmospheric CO2 enrichment on the mineral concentration of Citrus aurantium leaves. New Phytol 135:439–444

    Article  Google Scholar 

  • Peñuelas J, Filella I, Tognetti R (2001) Leaf mineral concentrations of Erica arborea, Juniperus communis and Myrtus communis growing in the proximity of a natural CO2 spring. Glob Change Biol 7:291–301

    Article  Google Scholar 

  • Pfirrmann T, Barnes JD, Steiner K, Schramel P, Busch U, Küchenhoff H, Payer HD (1996) Effects of elevated CO2, O and K deficiency on Norway spruce (Picea abies) nutrient supply, content and leaching. New Phytol 134:267–278

    CAS  Article  Google Scholar 

  • Piikki K, Vorne V, Ojanpera K, Pleijel H (2007) Impact of elevated O3 and CO2 exposure on potato (Solanum tuberosum L. cv. Bintje) tuber macronutrients (N, P, K, Mg, Ca). Agric Ecosyst Environ 118:55–64

    CAS  Article  Google Scholar 

  • Polley HW, Fay PA, Jin VL, Combs GF (in press) CO2 enrichment increases element concentrations in grass mixtures by changing species abundances. Plant Ecol. doi:10.1007/s11258-010-9874-y

  • Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198

    Article  Google Scholar 

  • Porter MA, Grodzinski B (1984) Acclimation to high CO2 in bean: carbonic anhydrase and ribulose bisphosphate carboxylase. Plant Physiol 74:413–416

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  • Prior SA, Torbert HA, Runion GB, Mullins GL, Rogers HH, Mauney JR (1998) Effects of carbon dioxide enrichment on cotton nutrient dynamics. J Plant Nutr 21:1407–1426

    CAS  Article  Google Scholar 

  • Prior SA, Runion GB, Rogers HH, Torbert HA (2008) Effects of atmospheric CO2 enrichment on crop nutrient dynamics under no-till conditions. J Plant Nutr 31:758–773

    CAS  Article  Google Scholar 

  • Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925

    CAS  PubMed  Article  Google Scholar 

  • Roberntz P, Stockfors J (1998) Effects of elevated CO2 concentration and nutrition on net photosynthesis, stomatal conductance and needle respiration of field-grown Norway spruce trees. Tree Phys 18:233–241

    Article  Google Scholar 

  • Rodenkirchen H, Göttlein A, Kozovits AR, Matyssek R, Grams TEE (2009) Nutrient contents and efficiencies of beech and spruce saplings as influenced by competition and O3/CO2 regime. Eur J For Res 128:117–128. doi:10.1007/s10342-008-0221-y

    CAS  Article  Google Scholar 

  • Rosenberg MS, Adams DC, Gurevitch J (2000) Meta-Win version 2.1: statistical software for meta-analysis. Sinauer Associates, Boston

    Google Scholar 

  • Rubio FW, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663

    CAS  PubMed  Article  Google Scholar 

  • Schlesinger WH (1997) Biogeochemistry: an analysis of global change. Academic Press, San Diego

    Google Scholar 

  • Seiler TJ, Rasse DP, Li J, Dijkstra P, Anderson HP, Johnson DP, Powell TL, Hungate BA, Hinkle CR, Drake BG (2009) Disturbance, rainfall and contrasting species responses mediated aboveground biomass response to 11 years of CO2 enrichment in a Florida scrub-oak ecosystem. Glob Change Biol 15:356–367

    Article  Google Scholar 

  • Seneweera SP, Conroy JP (1997) Growth, grain yield and quality of rice (Oryza sativa L.) in response to elevated CO2 and phosphorus nutrition. Soil Sci Plant Nutr 43:1131–1136

    CAS  Google Scholar 

  • Shinano T, Yamamoto T, Tawaraya K, Tadokoro M, Koike T, Osaki M (2007) Effects of elevated atmospheric CO2 concentration on the nutrient uptake characteristics of Japanese larch (Larix kaempferi). Tree Physiol 27:97–104

    CAS  PubMed  Article  Google Scholar 

  • Shipley B, Lechowicz M, Dumont S, Hendershot WH (1992) Interacting effects of nutrients, pH-Al and elevated CO2 on the growth of red spruce (Picea rubens Sarg.) seedlings. Water Air Soil Pollut 64:585–600

    CAS  Article  Google Scholar 

  • Silvester WB (1989) Molybdenum limitation of asymbiotic nitrogen fixation in forests of Pacific Northwest America. Soil Biol Biochem 21:283–289

    CAS  Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621

    CAS  Article  Google Scholar 

  • Suter D, Frehner M, Fischer BU, Nösberger J, Lüscher A (2002) Elevated CO2 increases carbon allocation to the roots of Lolium perenne under free-air CO2 enrichment but not in a controlled environment. New Phytol 154:65–75

    CAS  Article  Google Scholar 

  • Taiz L, Zeiger E (2002) Plant physiology, 3rd edn. Sinaeur Associates, Inc, Sunderland

    Google Scholar 

  • Taub DR, Wang X (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. J Integr Plant Biol 50:1365–1374

    CAS  PubMed  Article  Google Scholar 

  • Thomas RB, Richter DD, Ye H, Heine PR, Strain BR (1991) Nitrogen dynamics and growth of seedlings of an N-fixing tree (Gliricidia sepium (Jacq.) Walp.) exposed to elevated atmospheric carbon dioxide. Oecologia 88:415–421

    Article  Google Scholar 

  • Tremblay N, Yelle S, Gosselin A (1988) Effects of CO2 enrichment, nitrogen and phosphorus fertilization during the nursery period on mineral composition of celery. J Plant Nutr 11:37–49

    CAS  Article  Google Scholar 

  • Utriainen J, Janhunen S, Helmisaari HS, Holopainen T (2000) Biomass allocation, needle structural characteristics and nutrient composition in Scots pine seedlings exposed to elevated CO2 and O3 concentrations. Trees 14:475–484

    Article  Google Scholar 

  • van Groenigen KJ, Six J, Hungate BA, de Graaff MA, van Breemen N, van Kessel C (2006) Element interactions limit soil carbon storage. PNAS 103:6571–6574

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • Williams RJP, Frausto da Silva JJR (2002) The involvement of molybdenum in life. Biochem Biophys Res Commun 292:293–299

    CAS  PubMed  Article  Google Scholar 

  • Woodin S, Graham B, Killick A, Skiba U, Cresser M (1992) Nutrient limitation of the long-term response of heather [(Calluna vulgaris) L. Hull] to CO2 enrichment. New Phytol 122:635–642

    CAS  Article  Google Scholar 

  • Woodward FI (2002) Potential impacts of global elevated CO2 concentrations on plants. Curr Opin Plant Biol 5:207–211

    CAS  PubMed  Article  Google Scholar 

  • Wu DX, Wang GX, Bai YF, Liao JX (2004) Effects of elevated CO2 concentration on growth, water use, yield and grain quality of wheat under two soil water levels. Agric Ecosyst Environ 104:493–507

    Article  Google Scholar 

  • Yamakawa Y, Saigusa M, Okada M, Kobayashi K (2004) Nutrient uptake by rice and soil solution composition under atmospheric CO2 enrichment. Plant Soil 259:367–372

    CAS  Article  Google Scholar 

Download references

Acknowledgments

The authors sincerely thank Drs. Irakli Loladze, Andreas Fangmeier, Nicole Geissler, and their colleagues for sharing data. Dr. George Koch and Christina Bentrup provided enlightening conversations that clarified the interpretation of our results, and Dr. Walter G. Whitford provided valuable comments on an earlier manuscript. Dr. Craig Osenberg helped in clarifying variance calculations in the use of meta-analysis. J. Bradford McArtor contributed valuable infrastructure to B.D.D. A National Science Foundation-IGERT Fellowship supported B. D. D. during the preparation of the manuscript.

Author information

Author notes

  1. Benjamin D. Duval

    Present address: Energy Biosciences Institute, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

Authors and Affiliations

  1. Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, 86011, USA

    Benjamin D. Duval, Paul Dijkstra & Bruce A. Hungate

  2. School of Natural Sciences, University of California at Merced, Merced, CA, 95343, USA

    Joseph C. Blankinship

  3. Merriam Powell Center for Environmental Research, Flagstaff, AZ, 86011, USA

    Benjamin D. Duval, Paul Dijkstra & Bruce A. Hungate

Authors
  1. Benjamin D. Duval
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph C. Blankinship
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul Dijkstra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bruce A. Hungate
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamin D. Duval.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/s11258-015-0541-1.

This article has been retracted at the request of the authors because of multiple and unintentional data entry errors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11258_2011_9998_MOESM1_ESM.xls

Supporting Information Table 1: Dataset used in meta-analysis of elevated CO2 effects on leaf nutrient concentrations. Data collection procedure and analysis with Meta-Win (v. 2.1) are described in the Materials and Methods section of the text. (XLS 196 kb)

11258_2011_9998_MOESM2_ESM.xls

Supporting Information Table 2: Dataset used in meta-analysis of elevated CO2 effects on stem, root and grain nutrient concentrations. Data collection procedure and analysis with Meta-Win (v. 2.1) are described in the Materials and Methods section of the text. (XLS 100 kb)

11258_2011_9998_MOESM3_ESM.tiff

Supporting Information Figure 1: Evaluation of publication bias in our meta-analysis. Data points are the inverse of the standard deviation as a predictor of effect size. Symmetry around an effect size of zero suggests that there is not a publication bias toward positive or negative effects of elevated CO2 on plant nutrient concentrations in our dataset (Egger et al. 1997). (TIFF 1521 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Duval, B.D., Blankinship, J.C., Dijkstra, P. et al. RETRACTED ARTICLE: CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: a meta-analysis. Plant Ecol 213, 505–521 (2012). https://doi.org/10.1007/s11258-011-9998-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-011-9998-8

Keywords

  • Elevated CO2
  • Meta-analysis
  • Nitrogen status
  • Nutrients
  • Plant nutrition