Plant Ecology

, Volume 213, Issue 3, pp 505–521

RETRACTED ARTICLE: CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: a meta-analysis

  • Benjamin D. Duval
  • Joseph C. Blankinship
  • Paul Dijkstra
  • Bruce A. Hungate
Article

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.

Keywords

Elevated CO2 Meta-analysis Nitrogen status Nutrients Plant nutrition 

Supplementary material

11258_2011_9998_MOESM1_ESM.xls (196 kb)
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 (100 kb)
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 (1.5 mb)
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)

References

  1. Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. Springer, New YorkCrossRefGoogle Scholar
  2. 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 210:159–166CrossRefGoogle Scholar
  3. 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 121:403–412CrossRefGoogle Scholar
  4. 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 45:1267–1278CrossRefGoogle Scholar
  5. 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 48:1477–1486CrossRefGoogle Scholar
  6. Bazzaz FA (1990) The response of natural ecosystems to the rising global CO2 levels. Annu Rev Ecol Syst 21:167–196CrossRefGoogle Scholar
  7. Blank RR, Derner JD (2004) Effects of CO2 enrichment on plant-soil relationships of Lepidium latifolium. Plant Soil 262:159–167CrossRefGoogle Scholar
  8. 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 15:227–236CrossRefGoogle Scholar
  9. Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903PubMedCrossRefGoogle Scholar
  10. Brady NC, Weil RR (2002) The nature and properties of soils. Prentice Hall, Upper Saddle RiverGoogle Scholar
  11. Campbell CD, Sage RF (2002) Effects of CO2 and P on proteoid root formation in white lupin (Lupinus albus). Plant Cell Environ 25:1051–1059CrossRefGoogle Scholar
  12. 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 20:871–881PubMedCrossRefGoogle Scholar
  13. Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. PNAS 104:4990–4995PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cheng W, Johnson DW (1998) Elevated CO2, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202:167–174CrossRefGoogle Scholar
  15. Cheng W, Sakai H, Yagi K, Hasegawa (2009) Interactions of elevated CO2 and night temperature on rice growth and yield. Agric For Meteorol 149:51–58Google Scholar
  16. Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Glob Change Biol 4:43–54CrossRefGoogle Scholar
  17. 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 12:2077–2091CrossRefGoogle Scholar
  18. 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 44:221–230Google Scholar
  19. Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639PubMedCrossRefGoogle Scholar
  20. 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 45:2570–2574PubMedCrossRefGoogle Scholar
  21. Ebersberger D, Niklaus PA, Kandeler E (2003) Long term CO2 enrichment stimulates N-mineralization and enzyme activities in calcareous grassland. Soil Biol Biochem 35:965–972CrossRefGoogle Scholar
  22. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634PubMedCentralPubMedCrossRefGoogle Scholar
  23. 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 96:43–59PubMedCrossRefGoogle Scholar
  24. 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 10:215–229CrossRefGoogle Scholar
  25. 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 17:353–368CrossRefGoogle Scholar
  26. Farrar JF, Jones DL (2000) The control of carbon acquisition by roots. New Phytol 147:43–53CrossRefGoogle Scholar
  27. 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 82:470–484Google Scholar
  28. 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 104:14014–14019PubMedCentralPubMedCrossRefGoogle Scholar
  29. Fuhrer J (2003) Agroecosystem responses to combinations of elevated CO2, ozone, and global climate change. Agric Ecosyst Environ 97:1–20CrossRefGoogle Scholar
  30. 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 60:137–151Google Scholar
  31. Goldberg S, Forster HS, Godfrey CL (1996) Molybdenum adsorption on oxides, clay minerals and soils. SSSAJ 60:425–432CrossRefGoogle Scholar
  32. 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 37:1254–1262PubMedCrossRefGoogle Scholar
  33. Heagle AS, Miller JE, Sherrill DE, Rawlings JO (1993) Effects of ozone and carbon dioxide mixtures on two clones of white clover. New Phytol 123:751–762CrossRefGoogle Scholar
  34. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. Högy P, Fangmeier A (2009) Atmospheric CO2 enrichment affects potatoes: 2. Tuber quality traits. Eur J Agron 30:85–94CrossRefGoogle Scholar
  37. 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 70:141–152CrossRefGoogle Scholar
  38. 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 5:1–9CrossRefGoogle Scholar
  39. 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 47–62Google Scholar
  40. 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 304:1291PubMedCrossRefGoogle Scholar
  41. 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 75:207–216CrossRefGoogle Scholar
  42. Intergovernmental Panel on Climate Change (2007) 4th assessment synthesis report, AR4. Valencia, SpainGoogle Scholar
  43. 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 51:559–562CrossRefGoogle Scholar
  44. Jenny H (1980) The Soil Resource. Ecological Studies, vol 37. Springer-Verlag, New York, USACrossRefGoogle Scholar
  45. 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 13:1388–1399CrossRefGoogle Scholar
  46. 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 69:379–403CrossRefGoogle Scholar
  47. Kabata-Pendias A (2001) Trace elements in soils and plants. CRC Press, Boca Raton, FL, USAGoogle Scholar
  48. Keutgen N, Chen K (2001) Responses of citrus leaf photosynthesis, chlorophyll fluorescence, macronutrient and carbohydrate contents to elevated CO2. J Plant Physiol 158:1307–1316CrossRefGoogle Scholar
  49. 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 6:301–312CrossRefGoogle Scholar
  50. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540PubMedCrossRefGoogle Scholar
  51. 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 41:54–60CrossRefGoogle Scholar
  52. 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 10:55–62Google Scholar
  53. 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 177:352–361Google Scholar
  54. 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 17:343–351CrossRefGoogle Scholar
  55. Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? TREE 17:457–461Google Scholar
  56. 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 54:731–739CrossRefGoogle Scholar
  57. 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 28:733–749Google Scholar
  58. Lynch JP, Brown KM (2001) Topsoil foraging: an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237Google Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 54:175–185CrossRefGoogle Scholar
  61. 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 1–12Google Scholar
  62. 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 165:139–146CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 130:565–574CrossRefGoogle Scholar
  65. 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 5:455–470CrossRefGoogle Scholar
  66. 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 82:83–89PubMedCentralPubMedCrossRefGoogle Scholar
  67. 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 102:18052–18056PubMedCentralPubMedCrossRefGoogle Scholar
  68. 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 104:3–11CrossRefGoogle Scholar
  69. Oh N-W, Richter DD (2004) Soil acidification induced by elevated atmospheric CO2. Glob Change Biol 10:1936–1946CrossRefGoogle Scholar
  70. 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 CrossRefGoogle Scholar
  71. Overdieck D (1993) Elevated CO2 and the mineral content of herbaceous and woody plants. Vegetatio 104:403–411CrossRefGoogle Scholar
  72. 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 47:227–231CrossRefGoogle Scholar
  73. 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 101:31–38CrossRefGoogle Scholar
  74. 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 80:63–67PubMedCentralPubMedCrossRefGoogle Scholar
  75. 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 135:439–444CrossRefGoogle Scholar
  76. 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 7:291–301CrossRefGoogle Scholar
  77. 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 134:267–278CrossRefGoogle Scholar
  78. 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 118:55–64CrossRefGoogle Scholar
  79. 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
  80. Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198CrossRefGoogle Scholar
  81. Porter MA, Grodzinski B (1984) Acclimation to high CO2 in bean: carbonic anhydrase and ribulose bisphosphate carboxylase. Plant Physiol 74:413–416PubMedCentralPubMedCrossRefGoogle Scholar
  82. 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 21:1407–1426CrossRefGoogle Scholar
  83. 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 31:758–773CrossRefGoogle Scholar
  84. 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 440:922–925PubMedCrossRefGoogle Scholar
  85. 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 18:233–241CrossRefGoogle Scholar
  86. 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 CrossRefGoogle Scholar
  87. Rosenberg MS, Adams DC, Gurevitch J (2000) Meta-Win version 2.1: statistical software for meta-analysis. Sinauer Associates, BostonGoogle Scholar
  88. Rubio FW, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663PubMedCrossRefGoogle Scholar
  89. Schlesinger WH (1997) Biogeochemistry: an analysis of global change. Academic Press, San DiegoGoogle Scholar
  90. 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 15:356–367CrossRefGoogle Scholar
  91. 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 43:1131–1136Google Scholar
  92. 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 27:97–104PubMedCrossRefGoogle Scholar
  93. 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 64:585–600CrossRefGoogle Scholar
  94. Silvester WB (1989) Molybdenum limitation of asymbiotic nitrogen fixation in forests of Pacific Northwest America. Soil Biol Biochem 21:283–289CrossRefGoogle Scholar
  95. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  96. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621CrossRefGoogle Scholar
  97. 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 154:65–75CrossRefGoogle Scholar
  98. Taiz L, Zeiger E (2002) Plant physiology, 3rd edn. Sinaeur Associates, Inc, SunderlandGoogle Scholar
  99. 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 50:1365–1374PubMedCrossRefGoogle Scholar
  100. 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 88:415–421CrossRefGoogle Scholar
  101. 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 11:37–49CrossRefGoogle Scholar
  102. 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 14:475–484CrossRefGoogle Scholar
  103. van Groenigen KJ, Six J, Hungate BA, de Graaff MA, van Breemen N, van Kessel C (2006) Element interactions limit soil carbon storage. PNAS 103:6571–6574PubMedCentralPubMedCrossRefGoogle Scholar
  104. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  105. Williams RJP, Frausto da Silva JJR (2002) The involvement of molybdenum in life. Biochem Biophys Res Commun 292:293–299PubMedCrossRefGoogle Scholar
  106. 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 122:635–642CrossRefGoogle Scholar
  107. Woodward FI (2002) Potential impacts of global elevated CO2 concentrations on plants. Curr Opin Plant Biol 5:207–211PubMedCrossRefGoogle Scholar
  108. 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 104:493–507CrossRefGoogle Scholar
  109. Yamakawa Y, Saigusa M, Okada M, Kobayashi K (2004) Nutrient uptake by rice and soil solution composition under atmospheric CO2 enrichment. Plant Soil 259:367–372CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Benjamin D. Duval
    • 1
    • 3
    • 4
  • Joseph C. Blankinship
    • 2
  • Paul Dijkstra
    • 1
    • 3
  • Bruce A. Hungate
    • 1
    • 3
  1. 1.Department of Biological SciencesNorthern Arizona UniversityFlagstaffUSA
  2. 2.School of Natural SciencesUniversity of California at MercedMercedUSA
  3. 3.Merriam Powell Center for Environmental ResearchFlagstaffUSA
  4. 4.Energy Biosciences InstituteUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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