On a per-unit-biomass basis, Smart et al. (1998) noted there were no differences in the total amounts of nitrogen within CO2-enriched and ambiently-grown wheat seedlings after three weeks of exposure to atmospheric CO2 concentrations of 360 and 1,000 ppm. Nevertheless, the CO2-enriched seedlings exhibited greater rates of soil nitrate extraction than did the ambient-grown plants. Similarly, BassiriRad et al. (1998) reported that a doubling of the atmospheric CO2 concentration doubled the uptake rate of nitrate in the C4 grass Bouteloua eriopoda. However, they also reported that elevated CO2 had no effect on the rate of nitrate uptake in Prosopis, and that it actually decreased the rate of nitrate uptake by 55% in Larrea. Nonetheless, atmospheric CO2 enrichment increased total biomass in these two species by 55 and 69%, respectively. Thus, although the uptake rate of this nutrient was depressed under elevated CO2 conditions in the latter species, the much larger CO2-enriched plants likely still extracted more total nitrate from the soil than did the ambient-grown plants of the experiment.

It is also interesting to note that Nasholm et al. (1998) determined that trees, grasses and shrubs can all absorb significant amounts of organic nitrogen from soils. Thus, plants do not have to wait for the mineralization of organic nitrogen before they extract the nitrogen they need from soils to support their growth and development. Hence, the forms of nitrogen removed from soils by plants (nitrate vs. ammonium) and their abilities to remove different forms may not be as important as was once thought.

In another tree study, Finzi et al. (2002) found that, on average, loblolly pine that were exposed to an extra 200 ppm CO2 maintained rates of net primary productivity that were 25% greater, and produced 32% more biomass, than the trees growing in ambient air. Moreover, the elevated CO2 also increased the total amount of nitrogen present in the trees' biomass. In fact, the average annual requirement for nitrogen rose by 16% for the trees growing in the air enriched with CO2. In order to compensate for this increased nitrogen demand, the average uptake of nitrogen from the soil was enhanced by 28% in the CO2-enriched plot, which says a lot considering that soils in the study region are characteristically low in available nitrogen. In addition, average nitrogen-use efficiency rose by approximately 10% with atmospheric CO2 enrichment.

With respect to the uptake of phosphate, Staddon et al. (1999) reported that Plantago lanceolata and Trifolium repens plants grown at 650 ppm CO2 for 2.5 months exhibited total plant phosphorus contents that were much greater than those displayed by plants grown at 400 ppm CO2, due to the fact that atmospheric CO2 enrichment significantly enhanced plant biomass. Similarly, Rouhier and Read (1998) reported that enriching the air around Plantago lanceolata plants with an extra 190 ppm of CO2 for a period of three months led to increased uptake of phosphorus and greater tissue phosphorus concentrations than were observed in plants growing in ambient air.

Greater uptake of phosphorus can also occur due to CO2-induced increases in root absorptive surface area or enhancements in specific enzyme activities. In addressing the first of these phenomena, BassiriRad et al. (1998) reported that a doubling of the atmospheric CO2 concentration significantly increased the belowground biomass of Bouteloua eriopoda and doubled its uptake rate of phosphate. However, elevated CO2 had no effect on uptake rates of phosphate in Larrea and Prosopis. Because the CO2-enriched plants grew so much bigger, however, they still removed more phosphate from the soil on a per-plant basis. With respect to the second phenomenon, phosphatase - which is the primary enzyme responsible for the conversion of organic phosphate into usable inorganic forms - had its activity increased by 30 to 40% in wheat seedlings growing at twice-ambient CO2 concentrations (Barrett et al., 1998).

With respect to another nutrient, iron, Jin et al. (2009) grew twenty-day-old plants for an additional seven days within controlled-environment chambers maintained at atmospheric CO2 concentrations of either 350 or 800 ppm in an iron (Fe)-sufficient medium with a soluble Fe source or under Fe-limited conditions in a medium containing the sparingly soluble hydrous Fe(III)-oxide, while measuring a number of pertinent plant parameters. Results indicated that plant growth was increased by the elevated CO2 in both the Fe-sufficient and Fe-limited media, with shoot fresh weight increasing by 22% and 44%, respectively, and root fresh weight increasing by 43% and 97%, respectively. In addition, Jin et al. report that "the elevated CO2 under Fe-limited conditions enhance[d] root growth, root hair development, proton release, root FCR [ferric chelate reductase] activity, and expressions of LeFR01 and LeIRT1 genes [which respectively encode FCR and the Fe(II) transporter in tomato], all of which enable plants to access and accumulate more Fe." And they add, as would be expected, that "the associated increase in Fe concentrations in the shoots and roots alleviated Fe-deficiency-induced chlorosis."

In considering their results, Jin et al. write that the bioavailability of iron to terrestrial plants "is often limited (Guerinot and Yi, 1994), particularly in calcareous soils, which represent 30% of the earth's surface (Imsande, 1998)," and they thus conclude that "Fe nutrition in plants is likely to be affected by the continued elevation of atmospheric CO2, which, in turn, will affect crop production." And as their work strongly suggests, those important effects should be highly beneficial, while even wider biospheric benefits are suggested by the work of Sasaki et al. (1998), who demonstrated that both the ferric reductase activity and Fe uptake capacity of the marine alga Chlorococcum littorale cultured in Fe-limited media have been significantly enhanced by elevated CO2 concentrations.

In another study, Haase et al. (2008) grew barley (Hordeum vulgare L. cv. Europa) plants from seed for four weeks - both hydroponically in nutrient solution having adequate or less-than-adequate iron (Fe) concentrations (+Fe and -Fe, respectively), as well as in rhizobox microcosms filled with soil under the same two conditions of iron availability - in controlled-environment chambers maintained at atmospheric CO2 concentrations of either 400 or 800 ppm, while they measured a number of pertinent plant physiological parameters. This work revealed that the elevated atmospheric CO2 treatments stimulated biomass production in both Fe-sufficient and Fe-deficient barley plants, in both hydroponics and soil culture. In addition, they say there were three different CO2-induced modifications in plant activity: "(i) increased internal Fe use efficiency, (ii) stimulation of root growth, and (iii) increased root exudation of Fe-mobilizing phytosiderophores in the sub-apical root zones." And since phytosiderophores act as metal chelators that mobilize sparingly soluble inorganic forms of iron and zinc and make them more readily available to plants, the researchers suggest that atmospheric CO2 enrichment increases the competitiveness of plants such as barley with rhizosphere microorganisms in their quest for these often difficult-to-obtain trace elements, which phenomenon helps to explain the strong growth response of barley to atmospheric CO2 enrichment, even when iron availability is low.

As for studies dealing with multiple nutrients, Schaffer et al. (1997) grew two mango ecotypes, one evolving from a warm, humid tropical climate, and the other from a cool, dry subtropical region, for 12 months in glasshouses with atmospheres of either 350 or 700 ppm CO2 to determine the effects of CO2 enrichment on plant growth and leaf mineral nutrient concentrations. According to the researchers, although atmospheric CO2 enrichment led to partial photosynthetic acclimation in both ecotypes, greater net carbon gains were still achieved with elevated CO2, as indicated by greater plant dry mass values for trees grown at 700 ppm CO2. Elevated CO2 also tended to decrease foliar concentrations of mineral nutrients (N, P, K, Ca, Mg, S, Cl, Fe, Zn, Mn, Cu and B) in both mango cultivars, most likely due to a dilution effect, since atmospheric CO2 enrichment increased leaf dry mass. Yet, although the instantaneous doubling of the atmospheric CO2 content in this experiment reduced concentrations of leaf mineral elements, the authors stated that "given the slow rate at which global atmospheric CO2 concentration is increasing, it is possible that plants will adapt to elevated ambient CO2 concentrations over time with respect to mineral nutrition," as did sour orange trees after 85 months of exposure to elevated CO2 (Penuelas et al., 1997).

Several years later, Lieffering et al. (2004) analyzed the elemental concentrations of archived grain samples from temperate rice (Oryza sativa L. cv. Akitakomachi) crops they had grown previously under FACE conditions out-of-doors in a fertile agricultural field (Okada et al., 2001), where an approximate 200-ppm increase in the air's CO2 concentration increased rice grain yields by about 14% (Kim et al., 2003a,b).

Of the five macro-nutrients they measured (N, P, K, Mg, S), Lieffering et al. report that "only N showed a decrease in concentration with elevated CO2 in both years," while all six of the micro-nutrients studied (Zn Mn, Fe, Cu, B, Mo) exhibited concentration increases. For Zn and Mn, in particular, they say "there was a strong tendency [for concentrations] to increase," while the same could also have been said of Fe, which in the second year of the study exhibited a CO2-induced concentration increase on the order of 68%, as best as can be determined from Lieffering et al.'s bar graphs.

In concluding their paper, Lieffering et al. note that their study of the effects of elevated CO2 on grain elemental concentrations under real-world field conditions is "the first such report for a staple food crop: all other previously reported data were obtained from plants growing in pots and in some kind of enclosure." In contrast to the results obtained in most of these latter root-confining experiments, they note that, other than for N, "no dilution of [the] elements in the grain was observed, contrary to the general conclusions of Loladze (2002)." Hence, they conclude that "as long as there is a readily available supply of nutrients and that the nutrient uptake capacity response to elevated CO2 is equal [to] or greater than the whole plant biomass response [which was the case in their experiment, except for N], then no dilution should be observed."

Noting that "increased production of fine roots with CO2 enrichment (Norby et al., 2004; Pritchard et al., 2008) may allow plants to match increased carbon assimilation with increased uptake of soil-derived elements," Natali et al. (2009) "examined CO2 effects of 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)]."

The three U.S. researchers report that they "did not find an overall decline in foliar metal concentrations with CO2 enrichment," but that they did find that dilution effects for metal micronutrients were generally "less than for non-essential trace metals," and that "some essential plant metals were greater under elevated CO2 (for example, 28% increase in Mn across species and sites)." Natali et al. conclude that their results "should alleviate some concerns that rising CO2 concentrations will result in broad-scale decreases in the concentrations of all elements essential for plant function and animal nutrition," as proposed by Loladze (2002). They also say their generally opposite results for non-essential trace elements (some of which can be toxic) "may be applicable to contaminated systems," stating that "elevated CO2 may, through dilution effects, alleviate aluminum toxicity." In general, therefore, one could say that elevated CO2 tends to increase the availability of helpful trace elements, while it tends to decrease the availability of harmful ones.

Finally, in a somewhat different type of study, Urabe and Waki (2009) grew three algal species -- Scenedesmus obliquus (green algae), Cyclotella sp. (diatoms) and Synechococcus sp. (cyanobacteria) -- in mono- and mixed cultures at ambient (360 ppm) and high (2000 ppm) CO2 levels, and allowed a planktonic herbivore (Daphnia) to feed on the different algal populations thereby produced either individually or in various mixtures, to see if there was any CO2-induced effect on herbivore growth. In so doing, the two researchers report that "both in the mono- and mixed cultures, algal steady state abundance increased but algal P:C and N:C ratios decreased when they were grown at high CO2." They also found that "Daphnia fed monospecific algae cultured at high CO2 had decreased growth rates despite increased algal abundance." But "when fed mixed algae cultured at high CO2, especially consisting of diatoms and cyanobacteria or the three algal species," they found that "Daphnia maintained high growth rates despite lowered P and N contents relative to C in the algal diets." Such findings, in the words of Urabe and Waki, imply that "algal diets composed of multiple species can mitigate the adverse effects of elevated CO2 on herbivore performance," and that "in environments with high CO2, herbivores may find a new diet producer or a combination of producer species to best meet their nutritional demands."

In summary, as the CO2 content of the air increases, the experimental data that have been accumulated to date suggest that much of Earth's vegetation will likely display increases in biomass; and there is considerable evidence suggestive of the further likelihood that the larger plants thereby produced will develop more extensive root systems and extract greater amounts of mineral nutrients from the soils in which they are rooted, enabling them to sustain their enhanced growth.

References
Barrett, D.J., Richardson, A.E. and Gifford, R.M. 1998. Elevated atmospheric CO2 concentrations increase wheat root phosphatase activity when growth is limited by phosphorus. Australian Journal of Plant Physiology 25: 87-93.

BassiriRad, H., Reynolds, J.F., Virginia, R.A. and Brunelle, M.H. 1998. Growth and root NO3^- and PO4^3- uptake capacity of three desert species in response to atmospheric CO2 enrichment. Australian Journal of Plant Physiology 24: 353-358.

Finzi, A.C., DeLucia, E.H., Hamilton, J.G., Richter, D.D. and Schlesinger, W.H. 2002. The nitrogen budget of a pine forest under free air CO2 enrichment. Oecologia 132: 567-578.

Guerinot, M.L. and Yi, Y. 1994. Iron: nutritious, noxious, and not readily available. Plant Physiology 104: 815-820.

Haase, S., Rothe, A., Kania, A., Wasaki, J., Romheld, V., Engels, C., Kandeler, E. and Neumann, G. 2008. Responses to iron limitation in Hordeum vulgare L. as affected by the atmospheric CO2 concentration. Journal of Environmental Quality 37: 1254-1262.

Imsande, J. 1998. Iron, sulfur, and chlorophyll deficiencies: a need for an integrative approach in plant physiology. Physiologia Plantarum 103: 139-144.

Jin, C.W., Du, S.T., Chen, W.W., Li, G.X., Zhang, Y.S. and Zheng, S.J. 2009. Elevated carbon dioxide improves plant iron nutrition through enhancing the iron-deficiency-induced responses under iron-limited conditions in tomato. Plant Physiology 150: 272-280.

Kim, H.-Y., Lieffering, M., Kobayashi, K., Okada, M., Mitchell, M.W. and Gumpertz, M. 2003b. Effects of free-air CO2 enrichment and nitrogen supply on the yield of temperate paddy rice crops. Field Crops Research 83: 261-270.

Kim, H.-Y., Lieffering, M., Kobayashi, K., Okada, M. and Miura, S. 2003a. 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.

Lieffering, M., Kim, H.-Y., Kobayashi, K. and Okada, M. 2004. The impact of elevated CO2 on the elemental concentrations of field-grown rice grains. Field Crops Research 88: 279-286.

Loladze, I. 2002. Rising atmospheric CO2 and human nutrition: towards globally imbalanced plant stoichiometry. Trends in Ecology and Evolution 17: 457-461.

Nasholm, T., Ekblad, A., Nordin, A., Giesler, R., Hogberg, M. and Hogberg, P. 1998. Boreal forest plants take up organic nitrogen. Nature 392: 914-916.

Natali, S.M., Saņudo-Wilhelmy, S.A. and Lerdau, M.T. 2009. Plant and soil mediation of elevated CO2 impacts on trace metals. Ecosystems 12: 715-727.

Norby, R.J., Ledford, J., Reilly, C.D., Miller, N.E. and 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, USA 101: 9689-9693.

Okada, M., Lieffering, M., Nakamura, H., Yoshimoto, M., Kim. H.-Y. and Kobayashi, K. 2001. Free-air CO2 enrichment (FACE) using pure CO2 injection: system description. New Phytologist 150: 251-260.

Penuelas, J., Idso, S.B., Ribas, A. and Kimball, B.A. 1997. Effects of long-term atmospheric CO2 enrichment on the mineral concentration of Citrus aurantium leaves. New Phytologist 135: 439-444.

Pritchard, S.G., Strand, A.E., McCormack, M.L., Davis, M.A., Finzi, A., Jackson, R.B., Matamala, R., Rogers, H.H. and 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.

Rouhier, H. and Read, D.J. 1998. The role of mycorrhiza in determining the response of Plantago lanceolata to CO2 enrichment. New Phytologist 139: 367-373.

Sasaki, T., Kurano, N. and Miyachi, S. 1998. Induction of ferric reductase activity and of iron uptake capacity in Chlorococcum littorale cells under extremely high-CO2 and iron-deficient conditions. Plant & Cell Physiology 39: 405-410.

Schaffer, B., Whiley, A.W., Searle, C. and Nissen, R.J. 1997. Leaf gas exchange, dry matter partitioning, and mineral element concentrations in mango as influenced by elevated atmospheric carbon dioxide and root restriction. Journal of the American Society of Horticultural Science 122: 849-855.

Smart, D.R., Ritchie, K., Bloom, A.J. and Bugbee, B.B. 1998. Nitrogen balance for wheat canopies (Triticum aestivum cv. Veery 10) grown under elevated and ambient CO2 concentrations. Plant, Cell and Environment 21: 753-763.

Staddon, P.L., Fitter, A.H. and Graves, J.D. 1999. Effect of elevated atmospheric CO2 on mycorrhizal colonization, external mycorrhizal hyphal production and phosphorus inflow in Plantago lanceolata and Trifolium repens in association with the arbuscular mycorrhizal fungus Glomus mosseae. Global Change Biology 5: 347-358.

Urabe, J. and Waki, N. 2009. Mitigation of adverse effects of rising CO2 on a planktonic herbivore by mixed algal diets. Global Change Biology 15: 523-531.

Zak, D.R., Pregitzer, K.S., Curtis, P.S., Vogel, C.S., Holmes, W.E. and Lussenhop, J. 2000. Atmospheric CO2, soil-N availability, and allocation of biomass and nitrogen by Populus tremuloides. Ecological Applications 10: 34-46.