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Elevated CO2 Levels Affects the Concentrations of Copper and Cadmium in Crops Grown in Soil Contaminated with Heavy Metals under Fully Open-Air Field Conditions Hongyan Guo,†,‡,||,* Jianguo Zhu,‡,* Hui Zhou,† Yuanyuan Sun,§ Ying Yin,† Daping Pei,† Rong Ji,† Jichun Wu,§ and Xiaorong Wang† †
State Key Laboratory of Pollution Control and Resource Reuse, School of Environment, Nanjing University, Nanjing 210093, China State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Science, Nanjing 210008, China § State Key Laboratory of Pollution Control and Resource Reuse, School of Earth Sciences and Engineering, Hydrosciences Department, Nanjing University, Nanjing 210093, China Institute for Climate and Global Change Research (ICGCR), Nanjing University, Nanjing 210093, China
)
‡
bS Supporting Information ABSTRACT: Elevated CO2 levels and the increase in heavy metals in soils through pollution are serious problems worldwide. Whether elevated CO2 levels will affect plants grown in heavy-metal-polluted soil and thereby influence food quality and safety is not clear. Using a free-air CO2 enrichment (FACE) system, we investigated the impacts of elevated atmospheric CO2 on the concentrations of copper (Cu) or cadmium (Cd) in rice and wheat grown in soil with different concentrations of the metals in the soil. In the two-year study, elevated CO2 levels led to lower Cu concentrations and higher Cd concentrations in shoots and grain of both rice and wheat grown in the respective contaminated soil. Elevated CO2 levels slightly but significantly lowered the pH of the soil and led to changes in Cu and Cd fractionation in the soil. Our study indicates that elevated CO2 alters the distribution of contaminant elements in soil and plants, thereby probably affecting food quality and safety.
’ INTRODUCTION With increasing global industrialization, the atmospheric CO2 concentration has risen from approximately 280 μmol mol1 in preindustrial times to approximately 380 μmol mol1 now, and it is expected to continue increasing in the future.1 Elevated atmospheric CO2 levels can stimulate photosynthesis,2 enhance carbon deposition in soil,3 and change the rhizosphere conditions of the plant, leading to increases in biomass and yields of crops.46 Some industrial, mining, and agricultural activities have contaminated soils with heavy metals, and such pollution is increasingly becoming a serious environmental problem. In China, more than 2.0 107 ha of agricultural land is reportedly contaminated with heavy metals.7 Heavy metals are toxic to plants, animals, and humans at different concentrations, and are known to cause significant environmental damage and human health problems.710 Of the heavy metals, Cu is an essential micronutrient for plants and animals; however, when in excess, Cu can interfere with numerous physiological processes, resulting in cell toxicity. Cadmium is a toxic trace element in the environment that can be easily taken up by plants and subsequently transferred to humans through food chains. r 2011 American Chemical Society
In the future, further increases in global CO2 levels and contamination with heavy metals are likely. More research is needed to investigate the response of crops grown in soils contaminated with metals under elevated CO2 levels. In the few reports available, Duval et al.11 indicated that CO2 alters the distribution of contaminant elements in ecosystems; Wu et al.12 showed that elevated CO2 levels increases Cs concentrations in rice shoots and roots; and Li et al.13 reported that elevated CO2 levels decrease or barely affect Cu concentrations in six rice varieties grown in contaminated soils, but increase Cd levels in three rice varieties. These studies highlight the need for a better understanding of the mechanisms by which CO2 and heavy metals jointly affect crop growth and uptake of metals, especially from the viewpoint of food safety. One also must consider that these studies were conducted in open-top chambers (OTCs). Long et al.14 reported that the effects on plants grown in OTCs are often greater than on plants grown under open air. Therefore, the Received: January 14, 2011 Accepted: July 5, 2011 Revised: May 10, 2011 Published: July 19, 2011 6997
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way to approach such a study is to use free-air CO2 enrichment (FACE). FACE experiments are conducted in open fields, allow the best simulation of elevated CO2 environments,14 and have been carried out in many countries.5,15,16 With the aim of predicting future food safety, we used a fullsize (14 m diameter) FACE system in farm fields in Jiangsu Province, China to investigate the effect of elevated atmospheric CO2 on Cd and Cu levels on two important crops worldwide, rice and wheat.
’ MATERIALS AND METHODS
Figure 1. Copper concentrations in tissues of rice plants grown in soil with 0, 50, or 400 mg kg1 Cu added, under either ambient CO2 levels or elevated CO2 levels (FACE). (a) Rice shoots at the midtillering growth stage of the first rice sowing, (b) rice shoots at the panicle-initiation growth stage of the first rice sowing, (c) rice shoots at grain maturity of the first rice sowing, (d) rice seeds at grain maturity of the first rice sowing, (e) rice shoots at grain maturity of the second rice sowing, (f) rice seeds at grain maturity of the second rice sowing. Values represent means ( SD. An asterisk indicates a significant difference between FACE and ambient conditions (p < 0.05).
results of such studies cannot be extrapolated to address the effect of long-term, more realistic CO2 fumigation on plants. One
Experimental Site. The FACE system was established in the town of Xiaoji, Jiangdu County, Jiangsu Province, China (119°420 E, 32°350 N), where a rice-wheat rotation system is used. This region lies within the northern subtropic monsoon climate. The annual mean temperature is 1416 °C, and the mean annual precipitation is 980 mm. The annual length of the nonfrost period is approximately 220 days. The soil is Shajiang Aquic Cambosols with a sandyloamy texture. FACE System. The FACE system has been described in detail by Liu et al.17 and Okada et al.18 In brief, the FACE system consists of octagonal plots located in different paddies having similar soils and agronomic histories. The plots have either elevated CO2 levels (hereafter called FACE plots) or ambient CO2 conditions (hereafter called ambient plots). Each plot is ca. 80 m2. In the FACE plots, plants were exposed to elevated CO2 levels within rings 12.5 m in diameter that emitted pure CO2 from the periphery toward the center through emission tubes located about 5060 cm above the canopy. In the ambient plots, plants were grown under ambient CO2 conditions. To minimize CO2 contamination, ambient plots were at least 90 m away from the nearest FACE ring. The season-long average CO2 concentration of the ambient plots was about 370 μmol mol1. The CO2 concentration in the FACE plots was constantly controlled at about 200 μmol mol1 higher than in the ambient plots. Crop Cultivation and Sample Preparation. Rice (Oryza sativa L. cv. Wuxiangjing 14) and wheat (Triticum aestivum L. cv. Yangmai 14) plants were grown in plastic pots in soils collected from a local farm. The properties of the soils are shown in Supporting Information Table S1. Fresh soil was sieved through a 3 mm sieve and kept in the dark until used. Soils were spiked with either Cu or Cd; control soil was not spiked. Specified amounts of Cd in the form of a dissolved solution of CdCl2 3 2H2O were added and thoroughly mixed into the soil as 0, 0.5, and 2.0 mg kg1. Specified amounts of Cu in the form of a dissolved solution of CuSO4 3 5H2O were added and thoroughly mixed into soil as 0, 50, and 400 mg kg1. The spiked and unspiked soils were then watered to field water capacity and kept in the dark for six months. Prepared soil was placed in plastic pots (5 kg soil per pot; 20 cm in diameter, 35 cm in height). Two FACE plots and two ambient plots were used in this experiment; plants treated with Cu were grown on one FACE plot and one ambient plot, and plants treated with Cd were grown on another FACE plot and another ambient plot. Each treatment consisted of three replicate pots. The experiments were conducted from June 2006 to October 2008. A ricewheat rotation was used. The first rice seeds were planted in June 2006, and the plants were harvested in October 2006. The first wheat sowing was in November 2006, with harvest in May 2007. The second rice sowing was in June 2007, with harvest in October 2007. The second wheat sowing 6998
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was in November 2007, with harvest in May 2008. The third rice sowing was in June 2008. The rice and wheat plants from the first sowing were sampled at the midtillering, panicle-initiation, and grain-maturity growth stages, and those from the second sowing were only sampled at grain maturity. Soils were sampled at the rice grain-maturity growth stage of the second sowing (October 2007) for pH analysis and metal fractionations. Rice roots were sampled at the panicle-initiation stage of the third sowing and stored 40 °C for microscopy (August 2008). Determination of Cd and Cu. The sampled plants were thoroughly washed with tap water and then with deionized water, and were then oven-dried to a constant weight at 70 °C. The dried samples were ground, weighed, and digested with concentrated HNO3/HClO4 (4:1 v/v).19 The Cd and Cu concentrations in the digested solution were analyzed by atomic absorption spectroscopy (AAS; Thermo Sollar M6). Determination of Soil pH and Sequential Extraction of Soil. The pH of the soil was measured in a 0.01 M CaCl2 solution at a 1:2.5 ratio of soil to solution (w/v) using a pH meter. Copper and cadmium fractionation in soil was determined by sequential extraction using the method of the Commission of the European Communities (Community Bureau of Reference; BCR). The method is described in detail in Quevauviller et al.20 Scanning Electron Microscopy. Fresh rice roots were thoroughly washed with deionized water. The first 1 cm of each root tip was cut and coated with gold (ca. 1 nm thickness) for 60 s using a sputter coater (HITACH E-1010, Japan). The samples were viewed with a scanning electron microscope (SEM; S-3400N II, Hitachi, Japan). Statistics. Data are expressed as means ( standard deviation (n = 3; n represents three replicate pots) and analyzed statistically using the SPSS software program (SPSS Inc., version 16.0). The data were analyzed with a two-way analysis of variance (ANOVA) approach, that is, Cd or Cu treatment (three levels) and CO2 treatment (two levels). The mean values from the ambient plots were compared to the mean values from the FACE plots on each day of measurement using Tukey’s test. The difference between the means was considered significant at p < 0.05.
’ RESULTS AND DISCUSSION Copper Concentration in Plants. In our two-year study, elevated CO2 levels significantly led to lower a Cu concentration in both rice and wheat (Figures 1 and 2 and Supporting Information Table S2). At the midtillering stage of the first rice season, the Cu concentration in shoots of rice grown on FACE plots with 50 and 400 mg kg1 Cu in the soil were 23.0 and 22.9% lower, respectively, than in shoots of rice grown on ambient plots (Figure 1a, p < 0.05). At the panicle-initiation stage, the Cu concentration in shoots of rice grown on FACE plots with 50 mg kg1 Cu added was 22.2% lower than that in shoots of rice grown on ambient plots (Figure 1b, p < 0.05). At grain maturity of the first rice season, the Cu concentration in the shoots of rice grown on FACE plots was 34.1, 16.1, and 19.7% lower (Figure 1c, p < 0.05) than their counterparts grown on ambient plots with 0 (control), 50, and 400 mg kg1 Cu added, respectively, and the Cu concentration in the grains of rice grown on FACE plots with 400 mg kg1 Cu added to the soil (Figure 1d, p < 0.05) was 8.8% lower than in grains of rice grown on ambient plots. A similar trend was detected in samples from the second year. At grain
Figure 2. Copper concentrations in tissues of wheat plants grown in soil with 0, 50, or 400 mg kg1 Cu added, under either ambient CO2 levels or elevated CO2 levels (FACE). (a) Wheat shoots at the midtillering growth stage of the first wheat sowing, (b) wheat shoots at the panicleinitiation growth stage of the first wheat sowing, (c) wheat shoots at grain maturity of the first wheat sowing, (d) wheat seeds at grain maturity of the first wheat sowing, (e) wheat shoots at grain maturity of the second wheat sowing, and (f) wheat seeds at grain maturity of the second wheat sowing. Values represent means ( SD. An asterisk indicates a significant difference between FACE and ambient conditions (p < 0.05). 6999
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Figure 3. Cadmium concentrations in tissues of rice plants grown in soil with 0, 0.5, or 2.0 mg kg1 Cd added, under either ambient CO2 levels or elevated CO2 levels (FACE). (a) Rice shoots at the midtillering growth stage of the first rice sowing, (b) rice shoots at the panicle-initiation growth stage of the first rice sowing, (c) rice shoots at grain maturity of the first rice sowing, (d) rice seeds at grain maturity of the first rice sowing, (e) rice shoots at grain maturity of the second rice sowing, (f) rice seeds at grain maturity of the second rice sowing. Values represent means ( SD. An asterisk indicates a significant difference between FACE and ambient conditions (p < 0.05).
maturity of the second rice season, the Cu concentration in the shoots of rice grown on FACE plots with 0 (control) and
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400 mg kg1 Cu added was 18.6 and 12.6% (Figure 1e, p < 0.05) lower than shoots of rice grown on ambient plots, and the Cu concentration in the grains of rice grown on FACE plots with 0 (control), 50, and 400 mg kg1 Cu added was 25.5, 20.3, and 14.2% lower than in grains of rice grown on ambient plots (Figure 1f, p < 0.05). Similar results were observed for wheat (Figure 2). In previous studies of uncontaminated soils, Manderscheid et al.21 found that elevated CO2 levels led to lower concentrations of Ca, S, Mg, Fe, and Zn in the wheat grain; Fangmeier et al.22 reported that and elevated CO2 levels resulted in lower Ca, S, and Fe concentrations in spring wheat; and Yang et al.23 showed that the Cu content of milled rice grain under elevated CO2 levels was 20% lower than that of ambient atmosphere. In an OTC experiment with contaminated soils and elevated CO2 levels, Li et al.13 reported that the Cu concentration in rice grains was significantly lower than that of ambient atmosphere. In the short term, lower Cu concentrations in crops probably alleviate the Cu toxicity and have important positive implications for the food quality of crops harvested from contaminated soils with Cu. In our present study, the SEM images of rice roots showed that exposure to elevated CO2 levels alleviated Cu stress and increased the root hair density. When the plants were grown with 2 mg kg1 Cd on either FACE or ambient plots, the root hair density of rice was low (Supporting Information Figure S1). However, when the plants were grown with 400 mg kg1 Cu on FACE plots, the root hair density was markedly higher than that of plants grown on ambient plots with 400 mg kg1 Cu (Figure S1). In the long term, depending on the magnitude of the effect, Cu deficiency of crops has the potential to contribute to health problems. Cadmium Concentration in Plants. Elevated CO2 levels resulted in higher Cd concentrations in tissues of both wheat and rice, especially in those plants grown in soils contaminated with high levels of Cd (Figures 3 and 4, and Supporting Information Table S2). At the midtillering stage of the first rice season (Figure 3a), the Cd concentration in shoots of rice grown on the FACE and ambient plots did not significantly differ. At the panicle-initiation stage, the Cd concentrations in shoots of rice grown on FACE plots with 0.5 and 2 mg kg1 Cd were 55.7 and 7.8% higher, respectively, than in shoots of rice grown on ambient plots (Figure 3b, p < 0.05). At grain maturity of both the first and second rice season, the Cd concentration in shoots of rice grown on FACE plots with 2 mg kg1 Cd was 11.3 and 21.5% higher (p < 0.05), respectively, than in shoots of rice grown on ambient plots, but the Cd concentration in shoots of rice grown on FACE and ambient plots with 0 and 0.5 mg kg1 Cd did not significantly differ (Figure 3c, e). The Cd concentration in seeds was not significantly affected by elevated CO2 levels in the first rice season (Figure 3d). In the second rice season, the Cd concentration in seeds of plants grown on FACE plots with 2 mg kg1 Cd was 38.8% higher than in seeds of plants grown on ambient plots (p < 0.05), but the Cd concentration in seeds of rice grown on FACE and ambient plots with 0 and 0.5 mg kg1 Cd did not significantly differ (Figure 3f). Similar results were observed for wheat (Figure 4). In the present study, the Cd concentration in wheat grains of all samples far exceeded the legal limits (wheat flour: 0.1 mg kg1).24 The Cd concentration in rice seeds of the first and second seasons from plants grown on either FACE or ambient plots was below the legal limits (rice: 0.2 mg kg1).24 But after exposed to elevated CO2 level, the Cd concentration in 7000
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Figure 4. Cadmium concentrations in tissues of wheat plants grown in soil with 0, 0.5, or 2.0 mg kg1 Cd added, under either ambient CO2 levels or elevated CO2 levels (FACE). (a) Wheat shoots at the midtillering growth stage of the first wheat sowing, (b) wheat shoots at the panicle-initiation growth stage of the first wheat sowing, (c) wheat shoots at grain maturity of the first wheat sowing, (d) wheat seeds at grain maturity of the first wheat sowing, (e) wheat shoots at grain maturity of the second wheat sowing, (f) wheat seeds at grain maturity of the second wheat sowing. Values represent means ( SD. An asterisk indicates a significant difference between FACE and ambient conditions (p < 0.05).
rice seeds of second season is more close to the legal limits than that of the first season. Concerning such increasing trend of Cd
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concentrations in rice seeds under elevated CO2, the Cd concentration could exceed the legal limit in future seasons. Cadmium can accumulate in the human body and damage kidneys, bones, and reproductive system.25 To keep the Cd levels in creatinine in urine below 1 μg Cd g1 in 95% of the population by age 50, the European Food Safety Authority (EFSA) has suggested that the average daily dietary Cd intake should not exceed 0.36 μg Cd/kg body weight, which corresponds to a weekly dietary intake of 2.52 μg Cd/kg body weight.26 For an average adult of 60 kg with a daily intake of 261.1 g rice or wheat,27 this estimated weekly dietary intake would be far exceeded by all of the wheat samples from our study grown in control and contaminated soils and in rice samples grown in highly contaminated soil, and elevated CO2 levels significantly increased the Cd intake. Li et al.13 also found significantly higher Cd concentrations in three rice varieties grown on contaminated soils under elevated CO2 levels. In China, farmland polluted by Cd has reached 20 104 ha and produces 14.6 108 kg of agricultural products annually.28 Since almost the entire population in China currently depends on rice and wheat as staple foods, the high, toxic concentrations of Cd accumulated in crops threaten food quality and safety. This threat will increase as the CO2 levels increase in the future. Variations in Soil pH, and Cu and Cd Fractionation in Soil. After the second rice harvest (October 2007), the pH of the soil was slightly but significantly lower in the FACE plots than in the ambient plots (Supporting Information Table S3). Elevated CO2 levels also led to changes in Cu and Cd fractionation in the soil (Supporting Information Tables S4 and S5). Compared to soil from ambient plots, the acid-extractable fraction of Cu in soil from FACE plots with 50 and 400 mg kg1 Cu was 10.5 and 16.4% higher (p < 0.05), and the reducible fraction of Cu in soil from FACE plots was 6.7 and 7.9% lower (p < 0.05), respectively. Compared to the soil from ambient plots, the acid-extractable and reducible fractions of Cd in soil from FACE plots with 2 mg kg1 Cd were 4.7 and 6.9% higher (p < 0.05), and the oxidizable and residual fractions of Cd were 31.5 and 7.1% lower (p < 0.05), respectively. Several studies have indicated that elevated CO2 levels lower the pH of rhizosphere soils, favor the release of elements into soil solution, and as a result, help the plant to take up more elements. DeLucia et al.4 reported that elevated CO2 levels increased the concentration of oxalate in the soil, and that this low-molecularweight organic acid solubilized inorganic phosphorus, making it available for uptake by the plant. Andrews and Schlesinger15 observed an increase in cation concentration in the deep soil (200 cm) in the third year of CO2 fumigation, and proposed that the observed increases in cation availability were caused by the increased organic acid content. Wu et al.12 showed that elevated CO2 levels lowered the pH by 0.20.4 units compared to ambient CO2 levels, which implies that the lower pH in the rhizosphere zone could help the plants take up more Cs. Li et al.13 reported that the decrease in pH of 0.040.15 in the rhizosphere soil of rice was due to elevated CO2 levels, and considered that this slightly decreasing trend might be linked to higher Cd concentrations in rice. Cheng et al.29 reported that elevated CO2 levels significantly increased the concentration of Ca2+ and Mg2+ in soil solution and reduced the solution pH, and total cations in plant biomass were also significantly higher under elevated CO2 levels. In our study after the second rice harvest, especially for heavy-metal-contaminated soils, the pH of the soil also exhibited a decreasing trend and the acid-extractable fraction 7001
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Environmental Science & Technology of metals in soils exhibited an increasing trend at elevated CO2 levels. It is known that the mobility and bioavailability of heavy metals in the acid-extractable form are greater than that of other fractions.8 These changes can link elevated CO2 levels to the increasing phytoavailability of heavy metals and are probably sufficient to explain the higher Cd concentrations in rice and wheat in our study. Thus, we propose that at elevated CO2 levels, a pathway of alterations likely increases exudation of low-molecular-weight organic compounds by the roots of plants, lowers the pH of rhizosphere soils, changes the metal fractionation of rhizosphere soil, facilitates metal solubility and bioavailability, and increases uptake of metal by plants. But if the soils are contaminated with little or no Cd under elevated CO2 conditions, the slightly decrease in the pH of the soil will not lead to a significant uptake of Cd by crops. Since in our study the bioavailability of both Cu and Cd increased under elevated CO2 levels, we were surprised that Cd concentrations in the crops increased, but Cu concentrations decreased. There are a few possible explanations for these contrasting results. (1) Many studies have shown that elevated CO2 levels increase plant growth and yields,6,3032 including a study using a same FACE system that reported that elevated CO2 levels enhance hybrid rice grain yield by 34%.6 Recently, Duval et al.11 indicated that CO2 alters the distribution of contaminant elements in ecosystems, with contaminant elements accumulating in plants and declining in soil, both likely explained by the CO2 stimulation of plant biomass. Li et al.13 reported that although higher Cd concentrations and lower Cu concentration in rice grown on contaminated soils under elevated CO2 were detected, elevated CO2 still significantly increased the total uptake of Cu and Cd owing to the change in biomass. Similarly, the higher concentrations of Cd and lower concentrations of Cu in crops observed in our study were probably due to the change in biomass under elevated CO2 conditions, but not decreasing the uptake of Cu in crops. (2) As reported, elevated CO2 levels increased exudation of low-molecular-weight organic compounds by the roots of plants,4,15 but the binding strength of Cd and Cu to organic compounds differ.33 Copper has a relatively high binding affinity to organic matter, whereas Cd has a relatively weak affinity. This could have an influence on the uptake of Cd and Cu under elevated CO2 levels, leading to differences. (3) Cations, such as Ca2+, Mg2+, Na+, and K+, interfere with the heavy metal bioavailability and alleviate metal toxicity owing to cation competition.3437 Kinraide et al.38 reported that addition of Ca2+ and Mg2+ alleviates metal toxicity, but the relative ameliorative effectiveness of Ca2+ and Mg2+ depends upon the metal. Cheng et al.,29 who used a same FACE system, reported that elevated CO2 levels significantly stimulate Ca2+ and Mg2+ release from soil. In our study, increased Ca2+ and Mg2+ in solution in soil could have decreased both Cu and Cd uptake owing to cation competition, but the relative effectiveness for Cu and Cd could differ. Experimental evidence supporting the above explanations is lacking. Additional research is needed to investigate the relationship between elevated CO2 levels and the increased phytoavailability of heavy metals and to elucidate the different mechanisms of the uptake of these two metals. The data presented here were obtained from crops grown in artificially contaminated soils in pots. More data need to be collected from crops grown under a wide range of soil conditions and realistic field conditions to make better predictions on the combined effects of elevated CO2 levels and multimetal-contaminated soils on the metal uptake by
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crops and thereby on their contribution to food quality and safety at the world scale.
’ ASSOCIATED CONTENT
bS
Supporting Information. Tables S1S5, Figure S1. This material is available free of charge via the Internet at http://pubs. acs.org.
’ AUTHOR INFORMATION Corresponding Author
*Phone: +86-25-89680263; fax: +86-25-89680263. e-mail:
[email protected] (H. Y. Guo),
[email protected] (J. G. Zhu).
’ ACKNOWLEDGMENT This work was supported by the National Natural Science Foundation of China (grant no. 20777034 , 40110817 and 41030746), the Knowledge Innovation Program of Chinese Academy of Sciences (grant no. KZCX3-SW-440), the China Postdoctoral Science Foundation, and the Jiangsu Planned Projects for Postdoctoral Research Funds, and the Fundamental Research Funds for the Central Universities (grant no.1085021108). The main instruments and apparatus of the FACE system were supplied by the Japan National Institute for Agro-Environmental Sciences (NIAES) and the Japan Agricultural Research Centre for Tohoku Region (NARCT). ’ REFERENCES (1) IPCC. Summary for Policymakers. In Climate Change 2007; the Physical Science Basis, Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change; Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M., Miller, H. L., Eds.; Cambridge University Press: Cambridge, 2007. (2) Zhang, Y. B.; Duan, B. L.; Qiao, Y. Z.; Wang, K. Y.; Korpelainen, B.; Li, C. Y. Leaf photosynthesis of Betula albosinensis seedlings as affected by elevated CO2 and planting density. For. Ecol. Manage. 2008, 255, 1937–1944. (3) Hill, P. W.; Marshall, C.; Williams, G. G.; Blum, H.; Harmens, H.; Jones, D. L.; Farrar, J. F. The fate of photosynthetically-fixed carbon in Lolium perenne grassland as modified by elevated CO2 and sward management. New Phytol. 2007, 173, 766–777. (4) Delucia, E. H.; Callaway, R. M.; Thomas, E. M.; Schlesinger, W. H. Mechanisms of phosphorus acquisition for ponderosa pine seedlings under high CO2 and temperature. Ann. Bot. 1997, 79, 111–120. (5) Lieffering, M.; Kim, H. Y.; Kobayashi, K. The impact of elevated CO2 on the elemental concentrations of field-grown rice grains. Field Crops Res. 2004, 88, 279–286. (6) Liu, H. J.; Yang, L. X.; Wang, Y. L.; Huang, J. Y.; Zhu, J. G.; Wang, Y. X.; Dong, G. C.; Liu, G. Yield formation of CO2-enriched hybrid rice cultivar Shanyou 63 under fully open-air field conditions. Field Crops Res. 2008, 108, 93–100. (7) Huang, Y. Z.; Hu, Y.; Liu, Y. X. Combined toxicity of copper and cadmium to six rice genotypes (Oryza Sativa L.). J. Environ. Sci. 2009, 21, 647–653. (8) Mulligan, C. N.; Yong, R. N.; Gibbs, B. F. Remediation technologies for metal-contaminated soils and groundwater: An evaluation. Eng. Geol. 2001, 60, 193–207. (9) Nahmani, J.; Capowiez, Y.; Lavelle, P. Effects of metal pollution on soil macroinvertebrate burrow systems. Biol. Fertil. Soils 2005, 42, 31–39. 7002
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