, Volume 12, Issue 5, pp 715–727 | Cite as

Plant and Soil Mediation of Elevated CO2 Impacts on Trace Metals

  • Susan M. Natali
  • Sergio A. Sañudo-Wilhelmy
  • Manuel T. Lerdau


The cycling of trace metals through terrestrial ecosystems is modulated by plant and soil processes. Changes in plant growth and function and soil properties associated with increased atmospheric carbon dioxide (CO2) may therefore also affect the biological storage and stoichiometry of trace metals. We examined CO2 effects on a suite of metal micronutrients and contaminants in forest trees and soils at two free-air CO2 enrichment sites—a loblolly pine forest in North Carolina (Duke) and a sweetgum plantation in Tennessee [Oak Ridge National Laboratory (ORNL)]—and an open-top chamber experiment in a scrub-oak community in Florida [Smithsonian Environmental Research Center (SERC)]. We found that CO2 effects on soil metals were variable across sites; there were significantly higher surface soil metal concentrations with CO2 enrichment at Duke and ORNL (P < 0.05), but a trend of decreased soil metal concentrations at SERC (non-significant). These impacts on metals may be understood in the context of CO2 effects on soil organic matter (SOM); changes in percent SOM with CO2 enrichment were greatest at Duke (18% increase), followed by ORNL (7% increase), with limited effect at SERC (3% increase). There were significant effects of elevated CO2 on foliar metal concentrations at all sites, but the response of foliar metals to CO2 enrichment varied by metal, among sites, and within sites based on plant species, canopy height, and leaf age. Contrary to expectations, we did not find an overall decline in foliar metal concentrations with CO2 enrichment, and some essential plant metals were greater under elevated CO2 (for example, 28% increase in Mn across species and sites). Our results suggest that elevated CO2 impacts on trace metal biogeochemistry can be understood by accounting for both metal function (or lack thereof) in plants and the soil characteristics of the ecosystem.

Key words

biogeochemical cycles elevated CO2 free-air CO2 enrichment global change micronutrients soil organic matter trace metals 



We thank R. Norby, R. Oren, B. Hungate, and the staff at the FACE and SERC sites for field support, and K. Butterbach-Bahl and two anonymous reviewers for comments on this manuscript. This study was supported by grants from the U. S. Department of Energy, Office of Science (BER), and graduate fellowships from the National Science Foundation (S.M.N.) and Department of Energy (S.M.N.).

Supplementary material

10021_2009_9251_MOESM1_ESM.doc (162 kb)
(DOC 162 kb)


  1. 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 properties and plant production to rising CO2. New Phytologist 165: 351-371.PubMedCrossRefGoogle Scholar
  2. Andrews JA, Schlesinger WH. 2001. Soil CO2 dynamics, acidification, and chemical weathering in a temperate forest with experimental CO2 enrichment. Global Biogeochemical Cycles 15: 149-162.CrossRefGoogle Scholar
  3. Bradl HB. 2004. Adsorption of heavy metal ions on soils and soil constituents. Journal of Colloid and Interface Science 277: 1-18.PubMedCrossRefGoogle Scholar
  4. Carney KM, Hungate BA, Drake BG, Megonigal JP. 2007. Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proceedings of the National Academy of Sciences of the United States of America 104: 4990-4995.PubMedCrossRefGoogle Scholar
  5. Cotrufo MF, Ineson P, Scott A. 1998. Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biology 4: 43-54.CrossRefGoogle Scholar
  6. Curtis PS, Wang XZ. 1998. A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113: 299-313.CrossRefGoogle Scholar
  7. Dijkstra P, Hymus G, Colavito D, Vieglas DA, Cundari CM, Johnson DP, Hungate BA, Hinkle CR, Drake BG. 2002. Elevated atmospheric CO2 stimulates aboveground biomass in a fire-regenerated scrub-oak ecosystem. Global Change Biology 8: 90-103.CrossRefGoogle Scholar
  8. Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD. 2004. Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO(2) across four free-air CO2 enrichment experiments in forest, grassland and desert. Global Change Biology 10: 2121-2138.CrossRefGoogle Scholar
  9. Farquhar G, von Caemmerer S. (1982). Modelling of photosynthetic response to environmental conditions. In: Lange O, Nobel P, Osmond C, Ziegler H, (ed). Encyclopedia of plant physiology vol.12B: Physiological plant ecology II. New York: Springer-Verlag. p549-587.Google Scholar
  10. Filion M, Dutilleul P, Potvin C. 2000. Optimum experimental design for Free-Air Carbon dioxide Enrichment (FACE) studies. Global Change Biology 6: 843-854.CrossRefGoogle Scholar
  11. 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
  12. Hendrey GR, Ellsworth DS, Lewin KF, Nagy J. 1999. A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2. Global Change Biology 5: 293-309.CrossRefGoogle Scholar
  13. Hochberg Y. 1988. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75: 800-802.CrossRefGoogle Scholar
  14. Hungate BA, Stiling PD, Dijkstra P, Johnson DW, Ketterer ME, Hymus GJ, Hinkle CR, Drake BG. 2004. CO2 elicits long-term decline in nitrogen fixation. Science 304: 1291-1291.PubMedCrossRefGoogle Scholar
  15. Hymus GJ, Johnson DP, Dore S, Anderson HP, Hinkle CR, Drake BG. 2003. Effects of elevated atmospheric CO2 on net ecosystem CO2 exchange of a scrub-oak ecosystem. Global Change Biology 9: 1802-1812.CrossRefGoogle Scholar
  16. IPCC. 2007. Climate change 2007: The physical science basis. Solomon S, Qin D, Manning Z, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, editors. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. New York: Cambridge University Press. p996.Google Scholar
  17. Jastrow JD, Miller MR, Matamala R, Norby RJ, Boutton TW, Rice CW, Owensby CE. 2005. Elevated atmospheric carbon dioxide increases soil carbon. Global Change Biology 11: 2057-2064.CrossRefGoogle Scholar
  18. Johnson DW, Cheng W, Joslin JD, Norby RJ, Edwards NT, Todd Jr. DE. 2004. Effects of elevated CO2 on nutrient cycling in a sweetgum plantation. Biogeochemistry 69: 379–403.CrossRefGoogle Scholar
  19. Kalbitz K, Wennrich R. 1998. Mobilization of heavy metals and arsenic in polluted wetland soils and its dependence on dissolved organic matter. Science of the Total Environment 209: 27-39.PubMedCrossRefGoogle Scholar
  20. Linde M, Oborn I, Gustafsson JP. 2007. Effects of changed soil conditions on the mobility of trace metals in moderately contaminated urban soils. Water Air and Soil Pollution 183: 69-83.CrossRefGoogle Scholar
  21. Loladze I. 2002. Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends in Ecology & Evolution 17: 457-461.CrossRefGoogle Scholar
  22. Marschner H. 1995. Mineral nutrition of higher plants, 2nd edn. San Diego: Academic Press. 887p.Google Scholar
  23. McBride MB, Richards BK, Steenhuis T. 2004. Bioavailability and crop uptake of trace elements in soil columns amended with sewage sludge products. Plant and Soil 262: 71-84.CrossRefGoogle Scholar
  24. Natali SM, Sañudo-Wilhelmy SA, Norby R, Zhang H, Finzi A, Lerdau MT. 2008. Increased mercury in forest soils under elevated carbon dioxide. Oecologia 158: 343-354.PubMedCrossRefGoogle Scholar
  25. Norby RJ, Iversen CM. 2006. Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. Ecology 87: 5-14.PubMedCrossRefGoogle Scholar
  26. Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill E.G. 2004. Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proceedings of the National Academy of Sciences of the United States of America 101: 9689-9693.PubMedCrossRefGoogle Scholar
  27. Norby RJ, Todd DE, Fults J, Johnson DW. 2001. Allometric determination of tree growth in a CO2-enriched sweetgum stand. New Phytologist 150: 477-487.CrossRefGoogle Scholar
  28. Öborn I, Jansson G, Johnsson L. 1995. A field study on the influence of soil pH on trace element levels in spring wheat (Triticum aestivum), potatoes (Solanum tuberosum) and carrots (Daucus carota). Water, Air and Soil Pollution 85: 835-840.CrossRefGoogle Scholar
  29. Oh NH, Richter DD. 2004. Soil acidification induced by elevated atmospheric CO2. Global Change Biology 10:1936-1946.CrossRefGoogle Scholar
  30. Pritchard SG, Strand AE, McCormack ML, Davis MA, Finzi A, Jackson RB, Matamala R, Rogers HH, Oren R. 2008. Fine root dynamics in a loblolly pine forest are influenced by free-air-CO2-enrichment: a six-year-minirhizotron study. Global Change Biology 14:588-602.CrossRefGoogle Scholar
  31. Quinn G, Keough M. 2002. Experimental design and data analysis for biologists. New York: Cambridge University Press. 537p.Google Scholar
  32. Roth SK, Lindroth RL. 1995. Elevated atmospheric CO2 effects on phytochemistry, insect performance and insect parasitoid interactions. Global Change Biology 1: 173-182.CrossRefGoogle Scholar
  33. Sardans J, Peñuelas J, Estiarte M. 2008. Warming and drought change trace element bioaccumulation patterns in a Mediterranean shrubland. Chemosphere 70: 874–885.PubMedCrossRefGoogle Scholar
  34. Sardans J, Peñuelas, J. 2007. Drought changes the dynamics of trace element accumulation in a Mediterranean Quercus ilex forest. Environmental Pollution 147: 567-583.PubMedCrossRefGoogle Scholar
  35. Satterthwaite FE. 1946. An approximate distribution of estimates of variance components. Biometrics Bulletin 2: 110-114.CrossRefGoogle Scholar
  36. Scheiner SM. (2001). MANOVA: Multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J, (ed). Design and analysis of ecological experiments. New York: Oxford University Press. p99-115.Google Scholar
  37. Schmalzer PA, Hinkle CR. 1992. Recovery of oak-saw palmetto scrub after fire. Castanea 57: 158-173.Google Scholar
  38. Sholtis JD, Gunderson CA, Norby RJ, Tissue DT. 2004. Persistent stimulation of photosynthesis by elevated CO2 in a sweetgum (Liquidambar styraciflua) forest stand. New Phytologist 162: 343-354.CrossRefGoogle Scholar
  39. Sims JT. 1986. Soil-pH effects on the distribution and plant availability of manganese, copper, and zinc. Soil Science Society of America Journal 50: 367-373.CrossRefGoogle Scholar
  40. Sterner R, Elser J. (2002). Ecological stoichiometry: the biology of elements from molecules to the biosphere, Princeton. Princeton University Press. p439.Google Scholar
  41. Stiling P, Rossi AM, Hungate B, Dijkstra P, Hinkle CR, Knott WM, Drake B. 1999. Decreased leaf-miner abundance in elevated CO2: Reduced leaf quality and increased parasitoid attack. Ecological Applications 9: 240-244.PubMedGoogle Scholar
  42. Taub DR, Miller B, Allen H. 2008. Effects of elevated CO2 on the protein concentration of food crops: a meta-analysis. Global Change Biology 14: 565-575.CrossRefGoogle Scholar
  43. Taub DR, Wang X. 2008. Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypothesis. Journal of Integrative Plant Biology 50: 1365-1374.PubMedGoogle Scholar
  44. U.S. Environmental Protection Agency (1991) Method 200.3. Sample preparation procedure for spectrochemical determination of total recoverable elements in biological tissues. In: Methods for the determination of metals in environmental samplesGoogle Scholar
  45. U.S. Environmental Protection Agency (1996) Method 3050B. Acid digestion of sediments, sludges and soils. In: Test methods for evaluating solid waste, physical/chemical methodsGoogle Scholar
  46. Vanveen JA, Liljeroth E, Lekkerkerk LJA, Vandegeijn SC. 1991. Carbon fluxes in plant-soil systems at elevated atmospheric CO2 levels. Ecological Applications 1: 175-181.CrossRefGoogle Scholar
  47. Yachandra VK, Sauer K, Klein MP. 1996. Manganese cluster in photosynthesis: Where plants oxidize water to dioxygen. Chemical Reviews 96: 2927-2950.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Susan M. Natali
    • 1
  • Sergio A. Sañudo-Wilhelmy
    • 2
  • Manuel T. Lerdau
    • 3
  1. 1.Department of Botany & ZoologyUniversity of FloridaGainesvilleUSA
  2. 2.Marine and Environmental BiologyUniversity of Southern CaliforniaLos AngelesUSA
  3. 3.Departments of Environmental Sciences and BiologyUniversity of VirginiaCharlottesvilleUSA

Personalised recommendations