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PHYTOEXTRACTION POTENTIAL OF POPLAR (POPULUS ALBA L. VAR. PYRAMIDALIS BUNGE) FROM CALCAREOUS AGRICULTURAL SOILS CONTAMINATED BY CADMIUM Yahu Hu
a b
, Zhongren Nan
a b
, Cheng Jin
a b
, Ning Wang
a b
& Huanzhang Luo
a b
a
Key Laboratory of Western China's Environmental Systems , Ministry of Education, Lanzhou University , Lanzhou , 730000 , PR China b
College of Earth and Environmental Sciences , Lanzhou University , Lanzhou , 730000 , PR China Accepted author version posted online: 13 May 2013.
To cite this article: Yahu Hu , Zhongren Nan , Cheng Jin , Ning Wang & Huanzhang Luo (2013): PHYTOEXTRACTION POTENTIAL OF POPLAR (POPULUS ALBA L. VAR. PYRAMIDALIS BUNGE) FROM CALCAREOUS AGRICULTURAL SOILS CONTAMINATED BY CADMIUM, International Journal of Phytoremediation, DOI:10.1080/15226514.2013.798616 To link to this article: http://dx.doi.org/10.1080/15226514.2013.798616
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ACCEPTED MANUSCRIPT PHYTOEXTRACTION POTENTIAL OF POPLAR (POPULUS ALBA L. VAR. PYRAMIDALIS BUNGE) FROM CALCAREOUS AGRICULTURAL SOILS CONTAMINATED BY CADMIUM
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Yahu Hu, Zhongren Nan, Cheng Jin, Ning Wang, Huanzhang Luo
Key Laboratory of Western China’s Environmental Systems, Ministry of Education, Lanzhou University, Lanzhou 730000, PR China College of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, PR China
Address correspondence to ZR Nan, College of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, China. E-mail: [email protected]
Running head: PHYTOEXTRACTION OF POPLAR FOR CD FROM CALCAREOUS SOIL
To investigate the phytoextraction potential of Populus alba L. var. pyramidalis Bunge for cadmium (Cd) contaminated calcareous soils, a concentration gradient experiment and a field sampling experiment (involving poplars of different ages) were conducted. The translocation factors for all experiments and treatments were greater than 1. The bioconcentration factor decreased from 2.37 to 0.25 with increasing soil Cd concentration in the concentration gradient experiment and generally decreased with stand age under field conditions. The Cd
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ACCEPTED MANUSCRIPT concentrations in P. pyramidalis organs decreased in the order of leaves > stems > roots. The shoot biomass production in the concentration gradient experiment was not significantly reduced with soil Cd concentrations up to or slightly over 50 mg kg–1. The results show that the phytoextraction efficiency of P. pyramidalis depends on both the soil Cd concentration and the tree age. Populus pyramidalis is most suitable for remediation of slightly Cd contaminated
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calcareous soils through the combined harvest of stems and leaves under actual field conditions.
KEY WORDS: soil contamination, cadmium, phytoextraction, poplar, stand age INTRODUCTION Large areas of farmland have been contaminated by cadmium (Cd) from anthropogenic sources including atmospheric deposition, waste incineration, wastewater irrigation, mining and smelting, and agricultural application of sewage sludge, pesticides, and chemical fertilizers (Adriano 2001). In China, an estimated 1.3×104 ha of agricultural lands in 25 regions across 11 provinces has been contaminated with Cd (Chen et al. 1999). Cadmium is regarded as a priority contaminant in Chinese agricultural soils, because of the high input rate, averaging 0.004 mg Cd kg–1 yr–1 in the plough layer (0–20 cm) (Luo et al. 2009). Contamination of agricultural lands by Cd is a major concern because Cd is much more mobile than heavy metals such as copper (Cu) and lead (Pb) in soil and can easily be taken up by crops even at low concentrations (Renella et al. 2004). Thus, a current issue is identifying a suitable remediation method for Cd contaminated agricultural soils.
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ACCEPTED MANUSCRIPT Phytoextraction has been proposed as a possible remediation technology for cleaning up agricultural soils contaminated by heavy metals. Phytoremediation is considered to be cost-effective and environmentally-friendly compared with the conventional technologies used so far, which include excavation, burial, and soil washing (Raskin, Smith, and Salt 1997). Attention has recently been focused on determining the potential of woody plants such as trees for
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phytoextraction (Pulford and Watson 2003; Mertens et al. 2006). The major advantages of using trees for phytoextraction rather than hyperaccumulators and high biomass producing crop plants, are their relatively large biomasses (both root and shoot), fast growth rate, deep root systems, high transpiration rate, high metal tolerance and uptake, and ability to grow on nutrient-poor soils (Pulford and Watson 2003; Wuana and Okieimen 2011). Poplars, in particular, have shown a high tolerance and uptake to Cd (Laureysens et al. 2004; Wu et al. 2010; Lettens et al. 2011). The highest reported Cd concentration in poplar tissues is 209 mg kg–1, measured in the leaves of P. tricocapa × P. deltoides grown on a contaminated site with more than 300 mg Cd kg–1 (Robinson et al. 2000). Thus, poplars are regarded as a potential candidate to extract soil Cd. Recent studies have shown that several clones of Populus species have higher Cd removal potential at different Cd contamination levels (Komárek et al. 2008; Laureysens et al. 2004), but the phytoextraction potential of poplars along a soil Cd contamination gradient is largely unknown (Robinson et al. 2000; Wu et al. 2010). As deciduous perennial plants, the heavy metal concentrations in woody plants tend to change with stand age, in contrast to herbaceous hyperaccumulators (Mertens et al. 2006; Komárek et al. 2008). Thus, it is important to determine the performance of plants under field conditions in addition to short-term pot trial simulations, to identify an optimal rotation period for phytoextraction using tree plants.
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ACCEPTED MANUSCRIPT In calcareous soil in arid zones, the adsorption of Cd by CaCO3 and the low desorption rate caused by high pH leads to a relatively low Cd bioavailability (Sanchez-Camazano, Sanchez-Martin, and Lorenzo 1998; Yanai, Zhao, and McGrath 2006). Thus, relatively low Cd uptake levels by plants are always noted in calcareous soils compared with acid soils with equal soil Cd concentrations (Adriano 2001). Unfortunately, far fewer plants have been available for the
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phytoextraction of Cd contaminated calcareous soils. Therefore, screening for new species or clones with a higher Cd removal potential in calcareous soils is still a key part of phytoextraction, as the phytoextraction potential is known to differ both between and within tree species (Pulford and Watson 2003; Vandecasteele et al. 2003). The Baiyin region in Gansu Province is located in a calcareous soil zone in northern China, which has been a major non-ferrous metal mining and smelting base in China since the 1950s. Dongdagou is an escape canal in the Baiyin region that collected both domestic sewage and industrial wastewater discharged by non-ferrous metal mining and smelting plants and several other factories located in the mid to upper reaches of the canal. Agricultural land along this canal was irrigated with wastewater for 40 years from the 1960s. It is estimated that one third of the agricultural land along this canal has been heavily contaminated by Cd. The concentrations of Cd in agricultural soils along this canal range from 3.4 to 77.9 mg kg–1 (Liu 2003). The Cd concentrations measured in forage range from 5.4 to 32.7 mg kg–1 in corn, and in wheat grains from 1.98 to 4.12 mg kg–1; in the kidneys of sheep and cows concentrations were 25.39 and 27.2 mg kg–1, respectively (Liu 2003). The Cd concentrations measured in human hair and urine in this region were several times higher than in unpolluted regions (Gansu Environmental Monitoring Station 1984). After 2000, most of the agricultural land along this canal was abandoned, and
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ACCEPTED MANUSCRIPT poplar (Populus alba L. var. pyramidalis Bunge) was planted across large areas for revegetation and beautification. Populus pyramidalis is a variety of P. alba of which only male specimens have been identified. It is found widely in desert and arid regions of northwest China and is used for lumber production and ecological protection due to its fast growth rate, high biomass production, and
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elevated tolerance to stresses of drought, salt, and insects (Zhang et al. 2008). However, we have not found any reports on the Cd phytoextraction potential of P. pyramidalis in calcareous soils. In this paper, we aim to answer two questions: (1) Is the accumulation of Cd by P. pyramidalis different from other Populus species, based on either soil contamination level or soil type (calcareous soil and acid soils)? (2) Is the accumulation of Cd by P. pyramidalis in the field different from in pot trials because of the different growing conditions? MATERIALS AND METHODS Concentration Gradient Experiment Soil was collected from the plough layer (0–20 cm) of former agricultural soils near Heping in Yuzhong County, Gansu Province, northwest China, where Chinese loess is the parent material. The background Cd concentration in the soil is 0.6 mg kg–1, which is considered to be clean based on the grade B standard of the National Soil Environmental Quality Standard of China (GB15618–1995, 0.6 mg kg–1, for soil with pH > 7.5). The soil is a gray calcareous soil, classified as Calcisols by the IUSS Working Group WRB (2006). Prior to use, the soil was sieved through a 10 mm mesh. The detailed physico-chemical properties of the soil (Soil Y) are shown in Table 1. A concentration gradient experiment was established in the experimental station of the Key Laboratory of Arid and Grassland Agroecology, Ministry of Education, China. This station
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ACCEPTED MANUSCRIPT (104°09′04″E, 35°56′37″N) is at the Yuzhong campus of Lanzhou University, Gansu Province. The station has a temperate semiarid climate with a mean annual air temperature of 6.57°C and mean annual precipitation of 350 mm. Before planting, 7.5 kg of soil (dry weight) was uniformly mixed with cadmium nitrate [Cd(NO3)2] solution and fertilized with 0.25 g N kg–1 and 0.10 g P kg–1 (as NH4NO3 and K2HPO4,
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respectively) and placed into plastic pots (H = 26.5 cm, D = 22.5 cm) and equilibrated for two months. The bulk soils were watered with tap water (no metals detected) to approximately 50% of the maximum water holding capacity (WHC). There were three replicates for each of the six treatments including a control treatment (no Cd added) and five Cd concentrations (5, 10, 25, 50, and 100 mg kg–1). After incubation, two one-year-old P. pyramidalis plantlets at identical growth phases were planted in each pot in April 2011. The pots were kept outdoors in a natural field and were regularly watered with tap water to approximately 60% WHC to maintain optimal plant growth. In October, the plant roots, stems, and leaves were harvested separately. Field Sampling Experiment Minqin village (104°16′14″E, 36°29′41″N), which is located in the middle reach of the Dongdagou escape canal, was selected as the site of field sampling experiment. The meteorology at Minqin is similar to the site of pot trial. The mean Cd concentration in the soil is 29 mg kg–1, which is 97 times higher than the grade B standard (GB15618–1995, 0.3 mg kg–1, for soil with pH < 7.5). The soil type is the same as in the pot trial, with detailed soil properties given in Table 1 (Soil M). We divided the agricultural land (approximately 3.67 ha) evenly into three plots, and three complete plants of each stand age (three, five, and seven years) were sampled randomly from each
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ACCEPTED MANUSCRIPT plot in December 2010. The poplars grown on this site were cut for the first time. The plants were then separated into roots, stem wood and bark, and branches to determine the Cd concentrations and biomass yields in each part of the plant. We were unable to sample leaves because the autumn litter fall had been collected by local residents due to a lack of fuel. Pieces of the stem wood and bark were sampled at about 20%, 50%, and 80% of the total shoot height, and were subsequently
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pooled. Soil in the root zone (0–30 cm) of each plant was also collected at the same time to determine the total and the extractable Cd concentrations. Soil and Plant Analysis Plant samples were washed with deionized water, and then oven-dried at 75°C to a constant weight (about 48 h) and finely ground before analysis. Soil samples were air-dried and sieved to pass through a 2 mm mesh prior to analysis. About 1 g of each plant sample and 0.5 g of each soil sample were digested separately with a mixture of 70% HClO4 and 66% HNO3 (1:4 v/v) on a hot plate at 160°C for 5 h (Langer et al. 2009). The bioavailable Cd in soils was extracted by a 1 M NH4NO3 solution (Langer et al. 2009). The Cd concentrations in the digests and extracts were determined using an atomic absorption spectrophotometer (AAS, SOLAAR M6; Thermo Fisher Scientific, Waltham, MA, USA). Certified standard reference materials GBW 07603 (bush branches and leaves) and 07401 (dark brown soil), obtained from the Institute of Geophysical and Geochemical Exploration, CAGS (Hebei, China), were used to evaluate the accuracy and precision of the analysis. Our experimental results showed recoveries of 87–105% for the plant samples and 95–103% for the soil samples when compared with the certified values. The soil pH was determined using a pH meter (PHS-4, Jiangsu Manufactory of Electrical Analysis Instruments, Jiangyin, China) in a soil/water solution (1:2.5, w:v). The particle size
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ACCEPTED MANUSCRIPT distribution was determined using a MS-S3500 Microtrac sample delivery controller (Malvern, United Kingdom). The total carbonate content was determined by the gasometric method, and the soil organic matter content was determined using the K2Cr2O7 oxidation method (Bao 2000). Total soil N was measured with a Kjeltec System 2300 distilling unit (Tecator AB, Hoganas, Sweden) based on the Kjeldahl acid-digestion method. Total soil P was measured by the
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ammonium-molybdate method using a spectrophotometer (Nanodrop, Wilmington, Delaware USA) after digestion with concentrated H2SO4 and HClO4 on a hot plate. Calculations and Data Analysis The bioconcentration factor (BCF) is the ratio of the mean concentration of Cd in the plant shoots to the total concentration of Cd in the soil; and the translocation factor (TF) is the ratio of the mean concentration of Cd in the shoots to the roots (Wei, Zhou, and Mathews 2008). The percentage of NH4NO3-extractable Cd concentration to the total soil Cd concentration is referred as ‘% Cd extracted with NH4NO3 from total Cd in the soil’ (Mertens et al. 2006). The annual biomass yield was calculated by dividing the tissue dry weight of a given stand age by the corresponding stand age (Li et al. 2009). Data were analyzed by a one-way analysis of variance (ANOVA) followed by multiple comparisons using Duncan’s multiple-range test to separate means. All the values are expressed as mean ± SD (standard deviation). Statistical differences were considered to be significant at P < 0.05. All statistical analyses were performed using the SPSS 16.0 statistical package for Windows. All results are expressed on a dry weight basis. RESULTS
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ACCEPTED MANUSCRIPT Concentration Gradient Experiment Biomass production. The biomass production of P. pyramidalis with different Cd addition levels is shown in Figure 1. No visual symptoms of Cd toxicity were observed in aboveground tissues of P. pyramidalis during the course of the experiment. The leaf and shoot (stems + leaves) dry weights only decreased significantly compared with the control at 100 mg kg–1 added Cd,
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while there were no significant differences in the root and stem dry weights (P < 0.05). Cd concentration and mass in poplar tissues. As shown in Figure 2, the Cd concentration in P. pyramidalis tissues increased sharply with increasing Cd concentrations. The Cd concentrations in P. pyramidalis tissues tended to decrease in the order of leaves > stems > roots, with the highest concentration (35 mg kg–1) noted in leaves with 100 mg kg–1 added Cd. The mass of Cd in P. pyramidalis tissues increased significantly with increasing concentrations of added Cd (Figure 3). The leaves showed a smooth increase in mass with increasing concentrations of added Cd, in contrast to the roots and stems, due to the pronounced reduction in foliage production at the highest concentrations of added Cd (Figures 1 and 3). The mass of Cd in tissues of P. pyramidalis decreased in the order of stems > roots > leaves in both the control and the treatments with added Cd at 5, 10, 25, and 50 mg kg–1, while the 100 mg kg–1 added Cd treatment was in the order of roots > stems > leaves. The amount of Cd in the shoots accounted for 51–74% of the total Cd in the plant, with a maximum shoot Cd mass (1,111 µg plant–1) observed with 100 mg Cd kg–1 soil. Cadmium accumulation. The BCF and TF generally decreased with increasing Cd soil concentrations (Figure 4). Specifically, the BCF was greater than 1 only when the concentration of Cd in soil was ≤ 10 mg kg–1: the BCF was 2.37 for the control, 1.27 for 5 mg kg–1 added Cd, and
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ACCEPTED MANUSCRIPT 1.15 for 10 mg kg–1 added Cd. In contrast, the TF was greater than 1 for almost all treatments except for 100 mg kg–1 added Cd (TF = 0.94). Field Sampling Experiment Biomass production. Table 2 shows the annual biomass yield (calculated on stand age) of
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each plant part from the three stands. The annual biomass yield increased significantly with increasing stand age (P < 0.05), with the highest annual biomass yield for each plant part in the 7 yr old stand. Changes of Cd concentration and mass with stand age. As shown in Table 3, significant differences in Cd accumulation were found for the different tissues. The Cd concentration in the tissues generally decreased in the order of bark > branches > roots > stem wood, regardless of stand age. The Cd partitioning within poplar tissues was different for different stand ages (Table 3), with the 5 yr old stand having the highest Cd concentration in stem wood, branches, and shoots, averaging 9.45 mg kg–1, 28.16 mg kg–1, and 17.28 mg kg–1 respectively. The highest root and bark Cd concentrations occurred in the 3 yr old stand. The Cd concentrations in tissues of the 7 yr old stand were significantly lower than in the 3 yr and 5 yr old stands (P < 0.05). The annual Cd uptake (calculated on stand age) in the tissues of the different stands (Table 2) showed that the highest annual Cd uptake in the roots occurred in the 7 yr old stand, while the 5 yr old stand had the highest annual Cd uptakes by the stem, branch, and shoot. In the 5 yr old stand, the amount of Cd in the shoots (48.61 mg plant–1) accounted for 95% of the total Cd, which was a significantly higher proportion than in the 3 yr and 7 yr old stands (P < 0.05). Cadmium accumulation. As shown in Table 3, the highest BCF (0.60) and TF (1.27) values were both observed in the 5 yr old stand while the 7 yr old stand had the lowest BCF (0.32) and TF
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ACCEPTED MANUSCRIPT (1.01) values. Although the TFs for all stands were greater than one, the Cd availability in soil decreased with increasing stand age. The extractable Cd concentration under the 3 yr old plot was 5.21% of the total Cd concentration, but reduced to 4.37% and 4.09% under the 5 yr old and 7 yr old plots, respectively.
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DISCUSSION Plant Growth The biomass responses from the concentration gradient experiment showed that P. pyramidalis has a high tolerance to soil Cd, as plant growth was only significantly inhibited when 100 mg kg–1 Cd was added to soil. However, Robinson et al. (2000) found that poplar growth (Populus deltoides × P. yunnanensis NZ 5006) was significantly inhibited on soils (pH = 5.7) containing more than 20 mg Cd kg–1. Wu et al. (2010) also reported that low levels of added Cd (0.5 to 1.5 mg kg–1) in purple soils (2.95 mg Cd kg–1, pH = 4.85) caused a significant reduction in total poplar biomass (Populus deltoids × Populus nigra). These differences may be largely related to soil properties (calcareous soil in our research compared with acid soils in the other reports), as Cd is less available to plants in calcareous soils, and consequently had a relatively minor effect on plant growth (Adriano 2001). Populus pyramidalis is therefore capable of extracting Cd from soils with up to or slightly over 50 mg Cd kg–1 soil based on the expected tolerance capability of a hyperaccumulator (Wei et al. 2008). The biomass responses in the field show that the annual biomass yields of each plant part increased significantly with increasing stand age, showing extraordinarily rapid biomass development. This is consistent with the findings of Mertens et al. (2004) and Lettens et al. (2011) that an extremely high biomass development rate is the main characteristic for young trees in this
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ACCEPTED MANUSCRIPT stage. Consequently, a biological dilution effect on metal uptake may occur with increasing stand age (Pulford and Watson 2003). Thus, determining an optimal rotation period is particularly important when using woody plants for phytoextraction. Cadmium Concentration in Poplar Tissues Significant Cd accumulation differences in tissue were found in both the concentration
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gradient experiment and the field sampling experiment. We found that P. pyramidalis accumulated relatively high Cd concentrations in leaves compared with roots and stems, regardless of Cd soil concentrations. This trend is consistent with previous results obtained for Populus species clones screened by pot culture (Robinson et al. 2000; Komárek et al. 2008) and field sampling experiments (Laureysens et al. 2004; Lettens et al. 2011; Van Nevel et al. 2011). The highest Cd concentration measured in P. pyramidalis leaves (35 mg kg–1) was less than the 100 mg kg–1 that would be expected from a Cd hyperaccumulator (Baker et al. 2000). Thus, P. pyramidalis is not regarded as a Cd hyperaccumulator. However, the values measured in this study were much higher than the normal range of Cd concentrations in deciduous foliage (4–17 mg kg–1) collected from polluted areas around the world (Adriano 2001). Most importantly, at low soil Cd levels (≤ 10 mg kg–1), the Cd uptake was generally higher than has been reported for poplars grown on both calcareous and acid soils. For example, Madejón et al. (2004) found average Cd concentration of 3.82 mg kg–1 in leaves of white poplar trees from contaminated sites (4.29 mg Cd kg–1, pH < 7.5). Mertens et al. (2004) reported that white poplar accumulated 8.0 mg Cd kg–1 in its leaves on dredged soils (pH = 7.1) with 4.9–6.6 mg Cd kg–1. Wu et al. (2010) measured Cd concentration in leaves of Populus deltoids × Populus nigra ranging from 1.43 to 1.71 mg kg–1 on alluvial soils (2.87–4.27 mg Cd kg–1, pH = 8.02) and from 0.33 to
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ACCEPTED MANUSCRIPT 2.01 mg kg–1 on purple soils (2.95–4.35 mg Cd kg–1, pH = 4.85). Vollenweider, Menard, and Günthardt-Goerg (2011) measured Cd concentration of 13.3 mg kg–1 in leaves of Populus tremula on acid soils (10 mg Cd kg–1, pH = 6.4) spiked with filter dust and CdO. Compared with the studies reported above in wet regions, the relatively high Cd concentrations in P. pyramidalis leaves could be attributed to high water use under drought conditions. This is largely because a high
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transpiration rate has been demonstrated to be the main driving force for poplars to enhance the translocation of metals from roots to shoots (Robinson et al. 2000; Lettens et al. 2011). Our results suggest that P. pyramidalis is more suitable for remediating slightly Cd contaminated calcareous soils. The results also show that using poplars for the phytoextraction of Cd contaminated soils would require harvesting the litter fall at the end of the growing season to avoid the recycling of leaf bound Cd. In addition, a general trend of decreasing Cd concentrations with increasing stand age was observed during the field sampling experiment. This decrease might be related to both the decrease in bioavailable Cd concentrations in the root zone (Mertens et al. 2006; Li et al. 2009) and the dilution effect induced by rapid biomass development. Although the decreases in the total Cd concentrations of the soil were negligible, the Cd uptake probably represented the most soluble fraction (Mertens et al. 2006). The bark always accumulated much higher concentrations of Cd than the stem wood regardless of the stand age, suggesting that bark production is important. Cadmium Phytoextraction Potential of Populus pyramidalis The phytoextraction potential depends on both the dry aboveground biomass yield and the heavy metal concentration in the aboveground plant tissues (Neugschwandtner et al. 2008). We found that the amount of Cd in shoots increased significantly and considerably with increasing Cd
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ACCEPTED MANUSCRIPT addition levels, with the highest shoot amount (1,111 µg plant–1) measured in 100 mg Cd kg–1 soil. This value was higher than the corresponding shoot Cd amount noted for some Cd hyperaccumulators at the same concentration of added Cd (100 mg kg–1). For example, Ipomoea carnea and Brassica juncea accumulated Cd in shoots of 401 µg plant–1 and approximately 80 µg plant–1, respectively (Ghosh and Singh 2005), while approximately 60 µg plant–1 was accumulated
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by Taraxacum mongolicum (Wei et al. 2008). At low soil Cd levels, P. pyramidalis also showed greater Cd accumulation than some other poplar species such as Populus deltoids × Populus nigra grown on an alluvial soil (pH = 8.02) containing 4.37 mg kg–1 Cd (dry soil) which accumulated 304 µg Cd plant–1 in its shoots after 231 days (Wu et al. 2010). In the field experiment, we found the highest annual amount of Cd taken up by shoots occurred in the 5 yr old stand rather than the 3 yr and 7 yr old stands. This is consistent with previous studies on other fast growing tree plants; for example, Li et al. (2009) found that of 1, 2, 3, and 4 yr old stands of Averrhoa carambola, the 2 yr old stand had the highest Cd removal efficiency in field trials. Mertens et al. (2006) also found that a 2 yr old Salix fragilis had the highest annual Cd extraction rate out of 1, 2, 4, and 6 yr old stands. The field experiment results suggest that five years may be the optimal rotation period for P. pyramidalis. Previous studies (Robinson et al. 2000; Ghosh and Singh 2005; Mertens, Luyssaert, and Verheyen 2005; Langer et al. 2009) showed that the BCF decreased with increasing metal concentrations in the soil. That is, higher Cd accumulation in aboveground plant tissues compared with soil occurred at lower soil Cd concentrations, and this trend also occurred in our research. Plants with a BCF less than 1 for heavy metals are not considered appropriate for successful phytoextraction regardless of how large their achievable biomass is, due to the amount of time
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ACCEPTED MANUSCRIPT required for effective remediation (Ghosh and Singh 2005). Thus, successive phytoextraction must consider both the soil metal contamination level and the variation in phytoextraction potential with stand age. The results show that P. pyramidalis has a greater potential for phytoextraction of calcareous soils that are slightly contaminated by Cd, as it has a strong capability to translocate Cd from roots to shoots as seen in both pot culture and field sampling experiments.
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CONCLUSIONS The concentration gradient and field sampling experiments show that P. pyramidalis has an elevated tolerance to Cd with a critical tolerance concentration up to or slightly over 50 mg kg–1. In addition, P. pyramidalis is capable of translocating Cd from the roots to aerial parts of the plant with almost all TFs greater than 1. The BCF of P. pyramidalis generally decreased with increasing soil Cd concentration and stand age, but exceeded 1 when the soil Cd concentration was ≤ 10 mg kg–1, and peaking in the 5 yr old stand under field conditions. The highest Cd concentrations were noted in the poplar leaves, indicating that Cd removal would be more efficient if the leaves are harvested. Therefore, P. pyramidalis has a high phytoextraction potential for remediating slightly Cd contaminated calcareous soils. ACKNOWLEDGEMENT The research was supported by National Natural Science Foundation of China (NSFC 51178209 and 91025015), and the Scholarship Award for Excellent Doctoral Student granted by Lanzhou University, and the Fundamental Research Funds for the Central Universities in Lanzhou University (lzujbky-2012-141). REFERENCES
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ACCEPTED MANUSCRIPT Adriano DC. 2001. Trace elements in terrestrial environments: biogeochemistry, bioavailability and risks of metals. 2nd ed. New York: Springer-Verlag. p. 9–17, 267 and 276. Baker AJM, McGrath SP, Reeves RD, Smith JAC. 2000. Metal hyperaccumulator plants: A review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils. In: Terry N, Bañuelos G, eds. Phytoremediation of contaminated soil
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ACCEPTED MANUSCRIPT Laureysens I, Blust R, De Temmerman L, Lemmens C, Ceulemans R. 2004. Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture: I. Seasonal variation in leaf, wood and bark concentrations. Environ Pollut 131: 485–494. Lettens S, Vandecasteele B, De Vos B, Vansteenkiste D, Verschelde P. 2011. Intra- and inter-annual variation of Cd, Zn, Mn and Cu in foliage of poplars on contaminated soil. Sci
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Total Environ 409: 2306–2316. Li JT, Liao B, Dai ZY, Zhu R, Shu WS. 2009. Phytoextraction of Cd-contaminated soil by carambola (Averrhoa carambola) in field trials. Chemosphere 76: 1233–1239. Liu ZP. 2003. Lead poisoning combined with cadmium in sheep and horses in the vicinity of non-ferrous metal smelters. Sci Total Environ 309: 117–126. Luo L, Ma Y, Zhang S, Wei D, Zhu YG. 2009. An inventory of trace element inputs to agricultural soils in China. J Environ Manage 90: 2524–2530. Madejón P, Marañón T, Murillo JM, Robinson B. 2004. White poplar (Populus alba) as a biomonitor of trace elements in contaminated riparian forests. Environ Pollut 132: 145–155. Mertens J, Luyssaert S, Verheyen K. 2005. Use and abuse of trace metal concentrations in plant tissue for biomonitoring and phytoextraction. Environ Pollut 138: 1–4. Mertens J, Vervaeke P, De Schrijver A, Luyssaert S. 2004. Metal uptake by young trees from dredged brackish sediment: limitations and possibilities for phytoextraction and phytostabilisation. Sci Total Environ 326: 209–215. Mertens J, Vervaeke P, Meers E, Tack FMG. 2006. Seasonal changes of metals in willow (Salix sp.) stands for phytoremediation on dredged sediment. Environ Sci Technol 40: 1962–1968.
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ACCEPTED MANUSCRIPT Neugschwandtner RW, Tlustoš P, Komárek M, Száková J. 2008. Phytoextraction of Pb and Cd from a contaminated agricultural soil using different EDTA application regimes: Laboratory versus field scale measures of efficiency. Geoderma 114: 446–454. Pulford ID, Watson C. 2003. Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29: 529–540.
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Raskin I, Smith RD, Salt DE. 1997. Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8: 221–226. Renella G, Adamo P, Bianco MR, Landi L, Violante P, Nannipieri P. 2004. Availability and speciation of cadmium added to a calcareous soil under various managements. Eur J Soil Sci 55: 123–133. Robinson BH, Mills TM, Petit D, Fung LE, Green SR, Clothier BE. 2000. Natural and induced cadmium-accumulation in poplar and willow: Implications for phytoremediation. Plant Soil 227: 301–306. Sanchez-Camazano M, Sanchez-Martin MJ, Lorenzo LF. 1998. Significance of soil properties for content and distribution of cadmium and lead in natural calcareous soils. Sci Total Environ 218: 217–226. Vandecasteele B, Lauriks R, De Vos B, Tack FMG. 2003. Cd and Zn concentration in hybrid poplar foliage and leaf beetles grown on polluted sediment-derived soils. Environ Monit Assess 89: 263–283. Van Nevel L, Mertens J, Staelens J, De Schrijver A, Tack FMG, De Neve S, Meers E, Verheyen K. 2011. Elevated Cd and Zn uptake by aspen limits the phytostabilization potential compared to five other tree species. Ecol Eng 37: 1072–1080.
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ACCEPTED MANUSCRIPT Vollenweider P, Menard T, Günthardt-Goerg MS. 2011. Compartmentation of metals in foliage of Populus tremula grown on soils with mixed contamination. I. From the tree crown to leaf cell level. Environ Pollut 159: 324–336. Wei SH, Zhou QX, Mathews S. 2008. A newly found cadmium accumulator—Taraxacum mongolicum. J Hazard Mater 159: 544–547.
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Wuana RA, Okieimen FE. 2011. Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology, Doi:10.5402/2011/402647. Wu FZ, Yang WQ, Zhang J, Zhou LQ. 2010. Cadmium accumulation and growth responses of a poplar (Populus deltoids×Populus nigra) in cadmium contaminated purple soil and alluvial soil. J Hazard Mater 177: 268–273. Yanai J, Zhao FJ, McGrath SP. 2006. Effect of soil characteristics on Cd uptake by the hyperaccumulator Thlaspi caerulescens. Environ Pollut 139: 167–175. Zhang ZH, Kang XY, Wang SD, Li DL, Chen HW. 2008. Pollen development and multi-nucleate microspores of Populus pyramidalis Lauche. For Stud China 10: 107–111.
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Figure captions Figure 1 Biomass yields (expressed as dry weight) of poplar roots, stems, leaves, and shoots at different Cd addition concentrations (mean ± SD, n = 3). Means among the Cd addition concentrations for a given plant part having the same letter are not significantly different (P < 0.05). Figure 2 The Cd concentrations in roots, stems, leaves, and shoots of the poplar at different Cd addition concentrations (mean ± SD, n = 3). Values among the Cd addition concentrations for a given plant part having the same letter are not significantly different (P < 0.05). Figure 3 The Cd amounts in roots, stems, leaves, and shoots of the poplar at different Cd addition concentrations (mean ± SD, n = 3). Values among the Cd addition concentrations for a given plant part having the same letter are not significantly different (P < 0.05). Figure 4 Bioconcentration factor (BCF) and translocation factor (TF) of the poplar at different Cd addition concentrations.
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120
Root
Stem
Leaf
a
a
a
a 100
a
a a
-1 Dry biomass (g pot )
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Shoot
ab aa
a a
a
a
b a
a
80
a
60
40 ab
a
20
ab
b
b
c
0 0
5 10 25 50 -1 Cd addition concentrations (mg kg )
100
Figure 1
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ACCEPTED MANUSCRIPT -1 Cd concentration in poplar tissues (mg kg )
a
Root Stem Leaf Shoot
35 30
ab b
a
a
a
25 b 20
bc c
b
b b
15 c
c d
10 e
5 0
f
d
e
c
d
e d e
0
5 10 25 50 -1 Cd addition concentrations (mg kg )
100
Figure 2
2700 Root Stem Leaf Shoot
2400 2100 -1 Total Cd (µ g pot )
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40
a
a ab
a
b
1800
b b
1500
bc
c
1200
c
c
900
d
600
d d
300 d
e
e
cd a
a
a
a
b
c
0 0
5 10 25 50 -1 Cd addition concentrations (mg kg )
23
100
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ACCEPTED MANUSCRIPT Figure 3
BCF TF
2.5
Values for BCF and TF
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2.0
1.5
1.0
0.5
0.0 0
5 10 25 50 -1 Cd addition concentrations (mg kg )
100
Figure 4 Table 1 The physico-chemical properties and the total Cd content of the two soils used in this study (mean ± SD, n = 3)
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ACCEPTED MANUSCRIPT Soil M
Soil Y
Calcisols
Calcisols
Sand (0.05–2.00 mm)
44.48
38.06
Silt (0.002–0.05 mm)
46.07
57.51
Clay (< 0.002 mm)
9.45
4.43
Bulk density (g cm–3)
1.30
1.25
pH (H2O)
7.48 ± 0.04
7.50 ± 0.11
CaCO3 (g kg–1)
69.68 ± 0.02 72.04 ± 3.42
OM (g kg–1)
15.31 ± 1.05 12.42 ± 0.73
Total P (g kg–1)
1.46 ± 0.12
0.79 ± 0.01
Total N (g kg–1)
1.04 ± 0.03
0.92 ± 0.03
Cd (mg kg–1)
29 ± 1.43
0.6 ± 0.05
Soil type
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Particle size distribution (%)
Table 2 Annual biomass yields and annual amount of Cd uptake of the different poplar stands (mean ± SD, n = 9) Annual amount of Cd uptake (mg Stand
–1
Annual biomass yields (kg plant ) plant–1)
age
3 yr
Root
Stem
Branch
Shoot
Root
Stem Branch
0.15 ±
0.73 ±
0.23 ±
0.96 ±
2.27
9.58
c
c
c
c
25
5.54 ± b
Shoot 15.12 ± c
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0.07c
0.07c
0.07c
5 yr 0.20 ±
2.28 ±
0.53 ±
2.81 ±
0.02b
0.12b
0.04b
0.13b
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7 yr
±
±
0.09b
0.17c
2.79
33.61
±
±
0.14ab 3.63a 3.76
23.04 ±
0.41 ±
3.14 ±
0.95 ±
4.08 ±
±
0.07a
0.02a
0.08a
0.18a
0.28a
0.33b
0.50c
14.99
48.61 ±
± 0.43a
3.20a
14.54
37.58 ±
0.22b ± 2.50a
2.29b
Note: Shoots include roots, stems, and branches, leaves are not included. Means for a given plant part in the same column that are followed by the same letter are not significantly different (P < 0.05).
Table 3 Cd accumulating characteristics of poplar in field sampling experiment (mean ± SD, n = 9) Stand age
Cd concentration (mg kg–1)
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BC
TF
% Cd
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Woo
Bark
Branch
Shoot
F
extra
d
cted with NH4 NO3
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from total Cd in the soil 3 yr
5 yr
7 yr
14.95
8.43
±
±
35.00 ±
1.57a
0.85a
0.97a
13.65
9.45
±
±
27.37 ±
0.49a
0.79a
1.50b
9.07
4.84
±
±
19.03 ±
0.89b
0.39b
1.08c
24.35 ± 2.45a
28.16 ± 0.54a
15.85 ±
0.5
1.13a
5
17.28 ±
0.6
0.62a
0
1.06
1.27 5.21
15.30 ± 1.49b
9.20 ±
0.3
0.42b
2
4.37 1.01
4.09
Note: Shoots include woods, barks, and branches, leaves are not included. Values for a given plant part in the same column having the same letter are not significantly different (P < 0.05).
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International Journal of Phytoremediation Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/bijp20
PHYTOEXTRACTION POTENTIAL OF POPLAR (POPULUS ALBA L. VAR. PYRAMIDALIS BUNGE) FROM CALCAREOUS AGRICULTURAL SOILS CONTAMINATED BY CADMIUM Yahu Hu
a b
, Zhongren Nan
a b
, Cheng Jin
a b
, Ning Wang
a b
& Huanzhang Luo
a b
a
Key Laboratory of Western China's Environmental Systems , Ministry of Education, Lanzhou University , Lanzhou , 730000 , PR China b
College of Earth and Environmental Sciences , Lanzhou University , Lanzhou , 730000 , PR China Accepted author version posted online: 13 May 2013.
To cite this article: Yahu Hu , Zhongren Nan , Cheng Jin , Ning Wang & Huanzhang Luo (2013): PHYTOEXTRACTION POTENTIAL OF POPLAR (POPULUS ALBA L. VAR. PYRAMIDALIS BUNGE) FROM CALCAREOUS AGRICULTURAL SOILS CONTAMINATED BY CADMIUM, International Journal of Phytoremediation, DOI:10.1080/15226514.2013.798616 To link to this article: http://dx.doi.org/10.1080/15226514.2013.798616
Disclaimer: This is a version of an unedited manuscript that has been accepted for publication. As a service to authors and researchers we are providing this version of the accepted manuscript (AM). Copyediting, typesetting, and review of the resulting proof will be undertaken on this manuscript before final publication of the Version of Record (VoR). During production and pre-press, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal relate to this version also.
PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.
ACCEPTED MANUSCRIPT PHYTOEXTRACTION POTENTIAL OF POPLAR (POPULUS ALBA L. VAR. PYRAMIDALIS BUNGE) FROM CALCAREOUS AGRICULTURAL SOILS CONTAMINATED BY CADMIUM
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Yahu Hu, Zhongren Nan, Cheng Jin, Ning Wang, Huanzhang Luo
Key Laboratory of Western China’s Environmental Systems, Ministry of Education, Lanzhou University, Lanzhou 730000, PR China College of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, PR China
Address correspondence to ZR Nan, College of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, China. E-mail: [email protected]
Running head: PHYTOEXTRACTION OF POPLAR FOR CD FROM CALCAREOUS SOIL
To investigate the phytoextraction potential of Populus alba L. var. pyramidalis Bunge for cadmium (Cd) contaminated calcareous soils, a concentration gradient experiment and a field sampling experiment (involving poplars of different ages) were conducted. The translocation factors for all experiments and treatments were greater than 1. The bioconcentration factor decreased from 2.37 to 0.25 with increasing soil Cd concentration in the concentration gradient experiment and generally decreased with stand age under field conditions. The Cd
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ACCEPTED MANUSCRIPT concentrations in P. pyramidalis organs decreased in the order of leaves > stems > roots. The shoot biomass production in the concentration gradient experiment was not significantly reduced with soil Cd concentrations up to or slightly over 50 mg kg–1. The results show that the phytoextraction efficiency of P. pyramidalis depends on both the soil Cd concentration and the tree age. Populus pyramidalis is most suitable for remediation of slightly Cd contaminated
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calcareous soils through the combined harvest of stems and leaves under actual field conditions.
KEY WORDS: soil contamination, cadmium, phytoextraction, poplar, stand age INTRODUCTION Large areas of farmland have been contaminated by cadmium (Cd) from anthropogenic sources including atmospheric deposition, waste incineration, wastewater irrigation, mining and smelting, and agricultural application of sewage sludge, pesticides, and chemical fertilizers (Adriano 2001). In China, an estimated 1.3×104 ha of agricultural lands in 25 regions across 11 provinces has been contaminated with Cd (Chen et al. 1999). Cadmium is regarded as a priority contaminant in Chinese agricultural soils, because of the high input rate, averaging 0.004 mg Cd kg–1 yr–1 in the plough layer (0–20 cm) (Luo et al. 2009). Contamination of agricultural lands by Cd is a major concern because Cd is much more mobile than heavy metals such as copper (Cu) and lead (Pb) in soil and can easily be taken up by crops even at low concentrations (Renella et al. 2004). Thus, a current issue is identifying a suitable remediation method for Cd contaminated agricultural soils.
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ACCEPTED MANUSCRIPT Phytoextraction has been proposed as a possible remediation technology for cleaning up agricultural soils contaminated by heavy metals. Phytoremediation is considered to be cost-effective and environmentally-friendly compared with the conventional technologies used so far, which include excavation, burial, and soil washing (Raskin, Smith, and Salt 1997). Attention has recently been focused on determining the potential of woody plants such as trees for
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phytoextraction (Pulford and Watson 2003; Mertens et al. 2006). The major advantages of using trees for phytoextraction rather than hyperaccumulators and high biomass producing crop plants, are their relatively large biomasses (both root and shoot), fast growth rate, deep root systems, high transpiration rate, high metal tolerance and uptake, and ability to grow on nutrient-poor soils (Pulford and Watson 2003; Wuana and Okieimen 2011). Poplars, in particular, have shown a high tolerance and uptake to Cd (Laureysens et al. 2004; Wu et al. 2010; Lettens et al. 2011). The highest reported Cd concentration in poplar tissues is 209 mg kg–1, measured in the leaves of P. tricocapa × P. deltoides grown on a contaminated site with more than 300 mg Cd kg–1 (Robinson et al. 2000). Thus, poplars are regarded as a potential candidate to extract soil Cd. Recent studies have shown that several clones of Populus species have higher Cd removal potential at different Cd contamination levels (Komárek et al. 2008; Laureysens et al. 2004), but the phytoextraction potential of poplars along a soil Cd contamination gradient is largely unknown (Robinson et al. 2000; Wu et al. 2010). As deciduous perennial plants, the heavy metal concentrations in woody plants tend to change with stand age, in contrast to herbaceous hyperaccumulators (Mertens et al. 2006; Komárek et al. 2008). Thus, it is important to determine the performance of plants under field conditions in addition to short-term pot trial simulations, to identify an optimal rotation period for phytoextraction using tree plants.
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ACCEPTED MANUSCRIPT In calcareous soil in arid zones, the adsorption of Cd by CaCO3 and the low desorption rate caused by high pH leads to a relatively low Cd bioavailability (Sanchez-Camazano, Sanchez-Martin, and Lorenzo 1998; Yanai, Zhao, and McGrath 2006). Thus, relatively low Cd uptake levels by plants are always noted in calcareous soils compared with acid soils with equal soil Cd concentrations (Adriano 2001). Unfortunately, far fewer plants have been available for the
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phytoextraction of Cd contaminated calcareous soils. Therefore, screening for new species or clones with a higher Cd removal potential in calcareous soils is still a key part of phytoextraction, as the phytoextraction potential is known to differ both between and within tree species (Pulford and Watson 2003; Vandecasteele et al. 2003). The Baiyin region in Gansu Province is located in a calcareous soil zone in northern China, which has been a major non-ferrous metal mining and smelting base in China since the 1950s. Dongdagou is an escape canal in the Baiyin region that collected both domestic sewage and industrial wastewater discharged by non-ferrous metal mining and smelting plants and several other factories located in the mid to upper reaches of the canal. Agricultural land along this canal was irrigated with wastewater for 40 years from the 1960s. It is estimated that one third of the agricultural land along this canal has been heavily contaminated by Cd. The concentrations of Cd in agricultural soils along this canal range from 3.4 to 77.9 mg kg–1 (Liu 2003). The Cd concentrations measured in forage range from 5.4 to 32.7 mg kg–1 in corn, and in wheat grains from 1.98 to 4.12 mg kg–1; in the kidneys of sheep and cows concentrations were 25.39 and 27.2 mg kg–1, respectively (Liu 2003). The Cd concentrations measured in human hair and urine in this region were several times higher than in unpolluted regions (Gansu Environmental Monitoring Station 1984). After 2000, most of the agricultural land along this canal was abandoned, and
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ACCEPTED MANUSCRIPT poplar (Populus alba L. var. pyramidalis Bunge) was planted across large areas for revegetation and beautification. Populus pyramidalis is a variety of P. alba of which only male specimens have been identified. It is found widely in desert and arid regions of northwest China and is used for lumber production and ecological protection due to its fast growth rate, high biomass production, and
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elevated tolerance to stresses of drought, salt, and insects (Zhang et al. 2008). However, we have not found any reports on the Cd phytoextraction potential of P. pyramidalis in calcareous soils. In this paper, we aim to answer two questions: (1) Is the accumulation of Cd by P. pyramidalis different from other Populus species, based on either soil contamination level or soil type (calcareous soil and acid soils)? (2) Is the accumulation of Cd by P. pyramidalis in the field different from in pot trials because of the different growing conditions? MATERIALS AND METHODS Concentration Gradient Experiment Soil was collected from the plough layer (0–20 cm) of former agricultural soils near Heping in Yuzhong County, Gansu Province, northwest China, where Chinese loess is the parent material. The background Cd concentration in the soil is 0.6 mg kg–1, which is considered to be clean based on the grade B standard of the National Soil Environmental Quality Standard of China (GB15618–1995, 0.6 mg kg–1, for soil with pH > 7.5). The soil is a gray calcareous soil, classified as Calcisols by the IUSS Working Group WRB (2006). Prior to use, the soil was sieved through a 10 mm mesh. The detailed physico-chemical properties of the soil (Soil Y) are shown in Table 1. A concentration gradient experiment was established in the experimental station of the Key Laboratory of Arid and Grassland Agroecology, Ministry of Education, China. This station
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ACCEPTED MANUSCRIPT (104°09′04″E, 35°56′37″N) is at the Yuzhong campus of Lanzhou University, Gansu Province. The station has a temperate semiarid climate with a mean annual air temperature of 6.57°C and mean annual precipitation of 350 mm. Before planting, 7.5 kg of soil (dry weight) was uniformly mixed with cadmium nitrate [Cd(NO3)2] solution and fertilized with 0.25 g N kg–1 and 0.10 g P kg–1 (as NH4NO3 and K2HPO4,
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respectively) and placed into plastic pots (H = 26.5 cm, D = 22.5 cm) and equilibrated for two months. The bulk soils were watered with tap water (no metals detected) to approximately 50% of the maximum water holding capacity (WHC). There were three replicates for each of the six treatments including a control treatment (no Cd added) and five Cd concentrations (5, 10, 25, 50, and 100 mg kg–1). After incubation, two one-year-old P. pyramidalis plantlets at identical growth phases were planted in each pot in April 2011. The pots were kept outdoors in a natural field and were regularly watered with tap water to approximately 60% WHC to maintain optimal plant growth. In October, the plant roots, stems, and leaves were harvested separately. Field Sampling Experiment Minqin village (104°16′14″E, 36°29′41″N), which is located in the middle reach of the Dongdagou escape canal, was selected as the site of field sampling experiment. The meteorology at Minqin is similar to the site of pot trial. The mean Cd concentration in the soil is 29 mg kg–1, which is 97 times higher than the grade B standard (GB15618–1995, 0.3 mg kg–1, for soil with pH < 7.5). The soil type is the same as in the pot trial, with detailed soil properties given in Table 1 (Soil M). We divided the agricultural land (approximately 3.67 ha) evenly into three plots, and three complete plants of each stand age (three, five, and seven years) were sampled randomly from each
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ACCEPTED MANUSCRIPT plot in December 2010. The poplars grown on this site were cut for the first time. The plants were then separated into roots, stem wood and bark, and branches to determine the Cd concentrations and biomass yields in each part of the plant. We were unable to sample leaves because the autumn litter fall had been collected by local residents due to a lack of fuel. Pieces of the stem wood and bark were sampled at about 20%, 50%, and 80% of the total shoot height, and were subsequently
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pooled. Soil in the root zone (0–30 cm) of each plant was also collected at the same time to determine the total and the extractable Cd concentrations. Soil and Plant Analysis Plant samples were washed with deionized water, and then oven-dried at 75°C to a constant weight (about 48 h) and finely ground before analysis. Soil samples were air-dried and sieved to pass through a 2 mm mesh prior to analysis. About 1 g of each plant sample and 0.5 g of each soil sample were digested separately with a mixture of 70% HClO4 and 66% HNO3 (1:4 v/v) on a hot plate at 160°C for 5 h (Langer et al. 2009). The bioavailable Cd in soils was extracted by a 1 M NH4NO3 solution (Langer et al. 2009). The Cd concentrations in the digests and extracts were determined using an atomic absorption spectrophotometer (AAS, SOLAAR M6; Thermo Fisher Scientific, Waltham, MA, USA). Certified standard reference materials GBW 07603 (bush branches and leaves) and 07401 (dark brown soil), obtained from the Institute of Geophysical and Geochemical Exploration, CAGS (Hebei, China), were used to evaluate the accuracy and precision of the analysis. Our experimental results showed recoveries of 87–105% for the plant samples and 95–103% for the soil samples when compared with the certified values. The soil pH was determined using a pH meter (PHS-4, Jiangsu Manufactory of Electrical Analysis Instruments, Jiangyin, China) in a soil/water solution (1:2.5, w:v). The particle size
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ACCEPTED MANUSCRIPT distribution was determined using a MS-S3500 Microtrac sample delivery controller (Malvern, United Kingdom). The total carbonate content was determined by the gasometric method, and the soil organic matter content was determined using the K2Cr2O7 oxidation method (Bao 2000). Total soil N was measured with a Kjeltec System 2300 distilling unit (Tecator AB, Hoganas, Sweden) based on the Kjeldahl acid-digestion method. Total soil P was measured by the
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ammonium-molybdate method using a spectrophotometer (Nanodrop, Wilmington, Delaware USA) after digestion with concentrated H2SO4 and HClO4 on a hot plate. Calculations and Data Analysis The bioconcentration factor (BCF) is the ratio of the mean concentration of Cd in the plant shoots to the total concentration of Cd in the soil; and the translocation factor (TF) is the ratio of the mean concentration of Cd in the shoots to the roots (Wei, Zhou, and Mathews 2008). The percentage of NH4NO3-extractable Cd concentration to the total soil Cd concentration is referred as ‘% Cd extracted with NH4NO3 from total Cd in the soil’ (Mertens et al. 2006). The annual biomass yield was calculated by dividing the tissue dry weight of a given stand age by the corresponding stand age (Li et al. 2009). Data were analyzed by a one-way analysis of variance (ANOVA) followed by multiple comparisons using Duncan’s multiple-range test to separate means. All the values are expressed as mean ± SD (standard deviation). Statistical differences were considered to be significant at P < 0.05. All statistical analyses were performed using the SPSS 16.0 statistical package for Windows. All results are expressed on a dry weight basis. RESULTS
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ACCEPTED MANUSCRIPT Concentration Gradient Experiment Biomass production. The biomass production of P. pyramidalis with different Cd addition levels is shown in Figure 1. No visual symptoms of Cd toxicity were observed in aboveground tissues of P. pyramidalis during the course of the experiment. The leaf and shoot (stems + leaves) dry weights only decreased significantly compared with the control at 100 mg kg–1 added Cd,
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while there were no significant differences in the root and stem dry weights (P < 0.05). Cd concentration and mass in poplar tissues. As shown in Figure 2, the Cd concentration in P. pyramidalis tissues increased sharply with increasing Cd concentrations. The Cd concentrations in P. pyramidalis tissues tended to decrease in the order of leaves > stems > roots, with the highest concentration (35 mg kg–1) noted in leaves with 100 mg kg–1 added Cd. The mass of Cd in P. pyramidalis tissues increased significantly with increasing concentrations of added Cd (Figure 3). The leaves showed a smooth increase in mass with increasing concentrations of added Cd, in contrast to the roots and stems, due to the pronounced reduction in foliage production at the highest concentrations of added Cd (Figures 1 and 3). The mass of Cd in tissues of P. pyramidalis decreased in the order of stems > roots > leaves in both the control and the treatments with added Cd at 5, 10, 25, and 50 mg kg–1, while the 100 mg kg–1 added Cd treatment was in the order of roots > stems > leaves. The amount of Cd in the shoots accounted for 51–74% of the total Cd in the plant, with a maximum shoot Cd mass (1,111 µg plant–1) observed with 100 mg Cd kg–1 soil. Cadmium accumulation. The BCF and TF generally decreased with increasing Cd soil concentrations (Figure 4). Specifically, the BCF was greater than 1 only when the concentration of Cd in soil was ≤ 10 mg kg–1: the BCF was 2.37 for the control, 1.27 for 5 mg kg–1 added Cd, and
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ACCEPTED MANUSCRIPT 1.15 for 10 mg kg–1 added Cd. In contrast, the TF was greater than 1 for almost all treatments except for 100 mg kg–1 added Cd (TF = 0.94). Field Sampling Experiment Biomass production. Table 2 shows the annual biomass yield (calculated on stand age) of
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each plant part from the three stands. The annual biomass yield increased significantly with increasing stand age (P < 0.05), with the highest annual biomass yield for each plant part in the 7 yr old stand. Changes of Cd concentration and mass with stand age. As shown in Table 3, significant differences in Cd accumulation were found for the different tissues. The Cd concentration in the tissues generally decreased in the order of bark > branches > roots > stem wood, regardless of stand age. The Cd partitioning within poplar tissues was different for different stand ages (Table 3), with the 5 yr old stand having the highest Cd concentration in stem wood, branches, and shoots, averaging 9.45 mg kg–1, 28.16 mg kg–1, and 17.28 mg kg–1 respectively. The highest root and bark Cd concentrations occurred in the 3 yr old stand. The Cd concentrations in tissues of the 7 yr old stand were significantly lower than in the 3 yr and 5 yr old stands (P < 0.05). The annual Cd uptake (calculated on stand age) in the tissues of the different stands (Table 2) showed that the highest annual Cd uptake in the roots occurred in the 7 yr old stand, while the 5 yr old stand had the highest annual Cd uptakes by the stem, branch, and shoot. In the 5 yr old stand, the amount of Cd in the shoots (48.61 mg plant–1) accounted for 95% of the total Cd, which was a significantly higher proportion than in the 3 yr and 7 yr old stands (P < 0.05). Cadmium accumulation. As shown in Table 3, the highest BCF (0.60) and TF (1.27) values were both observed in the 5 yr old stand while the 7 yr old stand had the lowest BCF (0.32) and TF
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ACCEPTED MANUSCRIPT (1.01) values. Although the TFs for all stands were greater than one, the Cd availability in soil decreased with increasing stand age. The extractable Cd concentration under the 3 yr old plot was 5.21% of the total Cd concentration, but reduced to 4.37% and 4.09% under the 5 yr old and 7 yr old plots, respectively.
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DISCUSSION Plant Growth The biomass responses from the concentration gradient experiment showed that P. pyramidalis has a high tolerance to soil Cd, as plant growth was only significantly inhibited when 100 mg kg–1 Cd was added to soil. However, Robinson et al. (2000) found that poplar growth (Populus deltoides × P. yunnanensis NZ 5006) was significantly inhibited on soils (pH = 5.7) containing more than 20 mg Cd kg–1. Wu et al. (2010) also reported that low levels of added Cd (0.5 to 1.5 mg kg–1) in purple soils (2.95 mg Cd kg–1, pH = 4.85) caused a significant reduction in total poplar biomass (Populus deltoids × Populus nigra). These differences may be largely related to soil properties (calcareous soil in our research compared with acid soils in the other reports), as Cd is less available to plants in calcareous soils, and consequently had a relatively minor effect on plant growth (Adriano 2001). Populus pyramidalis is therefore capable of extracting Cd from soils with up to or slightly over 50 mg Cd kg–1 soil based on the expected tolerance capability of a hyperaccumulator (Wei et al. 2008). The biomass responses in the field show that the annual biomass yields of each plant part increased significantly with increasing stand age, showing extraordinarily rapid biomass development. This is consistent with the findings of Mertens et al. (2004) and Lettens et al. (2011) that an extremely high biomass development rate is the main characteristic for young trees in this
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ACCEPTED MANUSCRIPT stage. Consequently, a biological dilution effect on metal uptake may occur with increasing stand age (Pulford and Watson 2003). Thus, determining an optimal rotation period is particularly important when using woody plants for phytoextraction. Cadmium Concentration in Poplar Tissues Significant Cd accumulation differences in tissue were found in both the concentration
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gradient experiment and the field sampling experiment. We found that P. pyramidalis accumulated relatively high Cd concentrations in leaves compared with roots and stems, regardless of Cd soil concentrations. This trend is consistent with previous results obtained for Populus species clones screened by pot culture (Robinson et al. 2000; Komárek et al. 2008) and field sampling experiments (Laureysens et al. 2004; Lettens et al. 2011; Van Nevel et al. 2011). The highest Cd concentration measured in P. pyramidalis leaves (35 mg kg–1) was less than the 100 mg kg–1 that would be expected from a Cd hyperaccumulator (Baker et al. 2000). Thus, P. pyramidalis is not regarded as a Cd hyperaccumulator. However, the values measured in this study were much higher than the normal range of Cd concentrations in deciduous foliage (4–17 mg kg–1) collected from polluted areas around the world (Adriano 2001). Most importantly, at low soil Cd levels (≤ 10 mg kg–1), the Cd uptake was generally higher than has been reported for poplars grown on both calcareous and acid soils. For example, Madejón et al. (2004) found average Cd concentration of 3.82 mg kg–1 in leaves of white poplar trees from contaminated sites (4.29 mg Cd kg–1, pH < 7.5). Mertens et al. (2004) reported that white poplar accumulated 8.0 mg Cd kg–1 in its leaves on dredged soils (pH = 7.1) with 4.9–6.6 mg Cd kg–1. Wu et al. (2010) measured Cd concentration in leaves of Populus deltoids × Populus nigra ranging from 1.43 to 1.71 mg kg–1 on alluvial soils (2.87–4.27 mg Cd kg–1, pH = 8.02) and from 0.33 to
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ACCEPTED MANUSCRIPT 2.01 mg kg–1 on purple soils (2.95–4.35 mg Cd kg–1, pH = 4.85). Vollenweider, Menard, and Günthardt-Goerg (2011) measured Cd concentration of 13.3 mg kg–1 in leaves of Populus tremula on acid soils (10 mg Cd kg–1, pH = 6.4) spiked with filter dust and CdO. Compared with the studies reported above in wet regions, the relatively high Cd concentrations in P. pyramidalis leaves could be attributed to high water use under drought conditions. This is largely because a high
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transpiration rate has been demonstrated to be the main driving force for poplars to enhance the translocation of metals from roots to shoots (Robinson et al. 2000; Lettens et al. 2011). Our results suggest that P. pyramidalis is more suitable for remediating slightly Cd contaminated calcareous soils. The results also show that using poplars for the phytoextraction of Cd contaminated soils would require harvesting the litter fall at the end of the growing season to avoid the recycling of leaf bound Cd. In addition, a general trend of decreasing Cd concentrations with increasing stand age was observed during the field sampling experiment. This decrease might be related to both the decrease in bioavailable Cd concentrations in the root zone (Mertens et al. 2006; Li et al. 2009) and the dilution effect induced by rapid biomass development. Although the decreases in the total Cd concentrations of the soil were negligible, the Cd uptake probably represented the most soluble fraction (Mertens et al. 2006). The bark always accumulated much higher concentrations of Cd than the stem wood regardless of the stand age, suggesting that bark production is important. Cadmium Phytoextraction Potential of Populus pyramidalis The phytoextraction potential depends on both the dry aboveground biomass yield and the heavy metal concentration in the aboveground plant tissues (Neugschwandtner et al. 2008). We found that the amount of Cd in shoots increased significantly and considerably with increasing Cd
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ACCEPTED MANUSCRIPT addition levels, with the highest shoot amount (1,111 µg plant–1) measured in 100 mg Cd kg–1 soil. This value was higher than the corresponding shoot Cd amount noted for some Cd hyperaccumulators at the same concentration of added Cd (100 mg kg–1). For example, Ipomoea carnea and Brassica juncea accumulated Cd in shoots of 401 µg plant–1 and approximately 80 µg plant–1, respectively (Ghosh and Singh 2005), while approximately 60 µg plant–1 was accumulated
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by Taraxacum mongolicum (Wei et al. 2008). At low soil Cd levels, P. pyramidalis also showed greater Cd accumulation than some other poplar species such as Populus deltoids × Populus nigra grown on an alluvial soil (pH = 8.02) containing 4.37 mg kg–1 Cd (dry soil) which accumulated 304 µg Cd plant–1 in its shoots after 231 days (Wu et al. 2010). In the field experiment, we found the highest annual amount of Cd taken up by shoots occurred in the 5 yr old stand rather than the 3 yr and 7 yr old stands. This is consistent with previous studies on other fast growing tree plants; for example, Li et al. (2009) found that of 1, 2, 3, and 4 yr old stands of Averrhoa carambola, the 2 yr old stand had the highest Cd removal efficiency in field trials. Mertens et al. (2006) also found that a 2 yr old Salix fragilis had the highest annual Cd extraction rate out of 1, 2, 4, and 6 yr old stands. The field experiment results suggest that five years may be the optimal rotation period for P. pyramidalis. Previous studies (Robinson et al. 2000; Ghosh and Singh 2005; Mertens, Luyssaert, and Verheyen 2005; Langer et al. 2009) showed that the BCF decreased with increasing metal concentrations in the soil. That is, higher Cd accumulation in aboveground plant tissues compared with soil occurred at lower soil Cd concentrations, and this trend also occurred in our research. Plants with a BCF less than 1 for heavy metals are not considered appropriate for successful phytoextraction regardless of how large their achievable biomass is, due to the amount of time
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ACCEPTED MANUSCRIPT required for effective remediation (Ghosh and Singh 2005). Thus, successive phytoextraction must consider both the soil metal contamination level and the variation in phytoextraction potential with stand age. The results show that P. pyramidalis has a greater potential for phytoextraction of calcareous soils that are slightly contaminated by Cd, as it has a strong capability to translocate Cd from roots to shoots as seen in both pot culture and field sampling experiments.
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CONCLUSIONS The concentration gradient and field sampling experiments show that P. pyramidalis has an elevated tolerance to Cd with a critical tolerance concentration up to or slightly over 50 mg kg–1. In addition, P. pyramidalis is capable of translocating Cd from the roots to aerial parts of the plant with almost all TFs greater than 1. The BCF of P. pyramidalis generally decreased with increasing soil Cd concentration and stand age, but exceeded 1 when the soil Cd concentration was ≤ 10 mg kg–1, and peaking in the 5 yr old stand under field conditions. The highest Cd concentrations were noted in the poplar leaves, indicating that Cd removal would be more efficient if the leaves are harvested. Therefore, P. pyramidalis has a high phytoextraction potential for remediating slightly Cd contaminated calcareous soils. ACKNOWLEDGEMENT The research was supported by National Natural Science Foundation of China (NSFC 51178209 and 91025015), and the Scholarship Award for Excellent Doctoral Student granted by Lanzhou University, and the Fundamental Research Funds for the Central Universities in Lanzhou University (lzujbky-2012-141). REFERENCES
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ACCEPTED MANUSCRIPT Adriano DC. 2001. Trace elements in terrestrial environments: biogeochemistry, bioavailability and risks of metals. 2nd ed. New York: Springer-Verlag. p. 9–17, 267 and 276. Baker AJM, McGrath SP, Reeves RD, Smith JAC. 2000. Metal hyperaccumulator plants: A review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils. In: Terry N, Bañuelos G, eds. Phytoremediation of contaminated soil
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and water. Boca Raton Florida: Lewis Publishers. p. 85–107. Bao SD. 2000. Soil and agricultural chemistry analysis. Beijing: China Agriculture Press. p. 30–35 and 202–204. Chen H, Zheng CR, Tu C, Zhu YG. 1999. Heavy metal pollution in soils in China: status and countermeasures. Ambio 28: 130–134. Gansu Environmental Monitoring Station, Gansu Environmental Research Institute. 1984. The influence of cadmium pollutant upon the human being’s health in Baiyin city. Environ Res 1: 15–21 (in Chinese). Ghosh M, Singh SP. 2005. A comparative study of cadmium phytoextraction by accumulator and weed species. Environ Pollut 133: 365–371. IUSS Working Group WRB. 2006. World Soil Resources Reports No. 103. FAO, Rome. p. 74. Komárek M, Tlustoš P, Száková J, Chrastný V. 2008. The use of poplar during a two-year induced phytoextraction of metals from contaminated agricultural soils. Environ Pollut 151: 27–38. Langer I, Krpata D, Fitz WJ, Wenzel WW, Schweiger PF. 2009. Zinc accumulation potential and toxicity threshold determined for a metal-accumulating Populus canescens clone in a dose–response study. Environ Pollut 157: 2871–2877.
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ACCEPTED MANUSCRIPT Laureysens I, Blust R, De Temmerman L, Lemmens C, Ceulemans R. 2004. Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture: I. Seasonal variation in leaf, wood and bark concentrations. Environ Pollut 131: 485–494. Lettens S, Vandecasteele B, De Vos B, Vansteenkiste D, Verschelde P. 2011. Intra- and inter-annual variation of Cd, Zn, Mn and Cu in foliage of poplars on contaminated soil. Sci
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Total Environ 409: 2306–2316. Li JT, Liao B, Dai ZY, Zhu R, Shu WS. 2009. Phytoextraction of Cd-contaminated soil by carambola (Averrhoa carambola) in field trials. Chemosphere 76: 1233–1239. Liu ZP. 2003. Lead poisoning combined with cadmium in sheep and horses in the vicinity of non-ferrous metal smelters. Sci Total Environ 309: 117–126. Luo L, Ma Y, Zhang S, Wei D, Zhu YG. 2009. An inventory of trace element inputs to agricultural soils in China. J Environ Manage 90: 2524–2530. Madejón P, Marañón T, Murillo JM, Robinson B. 2004. White poplar (Populus alba) as a biomonitor of trace elements in contaminated riparian forests. Environ Pollut 132: 145–155. Mertens J, Luyssaert S, Verheyen K. 2005. Use and abuse of trace metal concentrations in plant tissue for biomonitoring and phytoextraction. Environ Pollut 138: 1–4. Mertens J, Vervaeke P, De Schrijver A, Luyssaert S. 2004. Metal uptake by young trees from dredged brackish sediment: limitations and possibilities for phytoextraction and phytostabilisation. Sci Total Environ 326: 209–215. Mertens J, Vervaeke P, Meers E, Tack FMG. 2006. Seasonal changes of metals in willow (Salix sp.) stands for phytoremediation on dredged sediment. Environ Sci Technol 40: 1962–1968.
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ACCEPTED MANUSCRIPT Neugschwandtner RW, Tlustoš P, Komárek M, Száková J. 2008. Phytoextraction of Pb and Cd from a contaminated agricultural soil using different EDTA application regimes: Laboratory versus field scale measures of efficiency. Geoderma 114: 446–454. Pulford ID, Watson C. 2003. Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29: 529–540.
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Raskin I, Smith RD, Salt DE. 1997. Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8: 221–226. Renella G, Adamo P, Bianco MR, Landi L, Violante P, Nannipieri P. 2004. Availability and speciation of cadmium added to a calcareous soil under various managements. Eur J Soil Sci 55: 123–133. Robinson BH, Mills TM, Petit D, Fung LE, Green SR, Clothier BE. 2000. Natural and induced cadmium-accumulation in poplar and willow: Implications for phytoremediation. Plant Soil 227: 301–306. Sanchez-Camazano M, Sanchez-Martin MJ, Lorenzo LF. 1998. Significance of soil properties for content and distribution of cadmium and lead in natural calcareous soils. Sci Total Environ 218: 217–226. Vandecasteele B, Lauriks R, De Vos B, Tack FMG. 2003. Cd and Zn concentration in hybrid poplar foliage and leaf beetles grown on polluted sediment-derived soils. Environ Monit Assess 89: 263–283. Van Nevel L, Mertens J, Staelens J, De Schrijver A, Tack FMG, De Neve S, Meers E, Verheyen K. 2011. Elevated Cd and Zn uptake by aspen limits the phytostabilization potential compared to five other tree species. Ecol Eng 37: 1072–1080.
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ACCEPTED MANUSCRIPT Vollenweider P, Menard T, Günthardt-Goerg MS. 2011. Compartmentation of metals in foliage of Populus tremula grown on soils with mixed contamination. I. From the tree crown to leaf cell level. Environ Pollut 159: 324–336. Wei SH, Zhou QX, Mathews S. 2008. A newly found cadmium accumulator—Taraxacum mongolicum. J Hazard Mater 159: 544–547.
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Wuana RA, Okieimen FE. 2011. Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology, Doi:10.5402/2011/402647. Wu FZ, Yang WQ, Zhang J, Zhou LQ. 2010. Cadmium accumulation and growth responses of a poplar (Populus deltoids×Populus nigra) in cadmium contaminated purple soil and alluvial soil. J Hazard Mater 177: 268–273. Yanai J, Zhao FJ, McGrath SP. 2006. Effect of soil characteristics on Cd uptake by the hyperaccumulator Thlaspi caerulescens. Environ Pollut 139: 167–175. Zhang ZH, Kang XY, Wang SD, Li DL, Chen HW. 2008. Pollen development and multi-nucleate microspores of Populus pyramidalis Lauche. For Stud China 10: 107–111.
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Figure captions Figure 1 Biomass yields (expressed as dry weight) of poplar roots, stems, leaves, and shoots at different Cd addition concentrations (mean ± SD, n = 3). Means among the Cd addition concentrations for a given plant part having the same letter are not significantly different (P < 0.05). Figure 2 The Cd concentrations in roots, stems, leaves, and shoots of the poplar at different Cd addition concentrations (mean ± SD, n = 3). Values among the Cd addition concentrations for a given plant part having the same letter are not significantly different (P < 0.05). Figure 3 The Cd amounts in roots, stems, leaves, and shoots of the poplar at different Cd addition concentrations (mean ± SD, n = 3). Values among the Cd addition concentrations for a given plant part having the same letter are not significantly different (P < 0.05). Figure 4 Bioconcentration factor (BCF) and translocation factor (TF) of the poplar at different Cd addition concentrations.
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120
Root
Stem
Leaf
a
a
a
a 100
a
a a
-1 Dry biomass (g pot )
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Shoot
ab aa
a a
a
a
b a
a
80
a
60
40 ab
a
20
ab
b
b
c
0 0
5 10 25 50 -1 Cd addition concentrations (mg kg )
100
Figure 1
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ACCEPTED MANUSCRIPT -1 Cd concentration in poplar tissues (mg kg )
a
Root Stem Leaf Shoot
35 30
ab b
a
a
a
25 b 20
bc c
b
b b
15 c
c d
10 e
5 0
f
d
e
c
d
e d e
0
5 10 25 50 -1 Cd addition concentrations (mg kg )
100
Figure 2
2700 Root Stem Leaf Shoot
2400 2100 -1 Total Cd (µ g pot )
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40
a
a ab
a
b
1800
b b
1500
bc
c
1200
c
c
900
d
600
d d
300 d
e
e
cd a
a
a
a
b
c
0 0
5 10 25 50 -1 Cd addition concentrations (mg kg )
23
100
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BCF TF
2.5
Values for BCF and TF
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2.0
1.5
1.0
0.5
0.0 0
5 10 25 50 -1 Cd addition concentrations (mg kg )
100
Figure 4 Table 1 The physico-chemical properties and the total Cd content of the two soils used in this study (mean ± SD, n = 3)
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ACCEPTED MANUSCRIPT Soil M
Soil Y
Calcisols
Calcisols
Sand (0.05–2.00 mm)
44.48
38.06
Silt (0.002–0.05 mm)
46.07
57.51
Clay (< 0.002 mm)
9.45
4.43
Bulk density (g cm–3)
1.30
1.25
pH (H2O)
7.48 ± 0.04
7.50 ± 0.11
CaCO3 (g kg–1)
69.68 ± 0.02 72.04 ± 3.42
OM (g kg–1)
15.31 ± 1.05 12.42 ± 0.73
Total P (g kg–1)
1.46 ± 0.12
0.79 ± 0.01
Total N (g kg–1)
1.04 ± 0.03
0.92 ± 0.03
Cd (mg kg–1)
29 ± 1.43
0.6 ± 0.05
Soil type
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Particle size distribution (%)
Table 2 Annual biomass yields and annual amount of Cd uptake of the different poplar stands (mean ± SD, n = 9) Annual amount of Cd uptake (mg Stand
–1
Annual biomass yields (kg plant ) plant–1)
age
3 yr
Root
Stem
Branch
Shoot
Root
Stem Branch
0.15 ±
0.73 ±
0.23 ±
0.96 ±
2.27
9.58
c
c
c
c
25
5.54 ± b
Shoot 15.12 ± c
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0.07c
0.07c
0.07c
5 yr 0.20 ±
2.28 ±
0.53 ±
2.81 ±
0.02b
0.12b
0.04b
0.13b
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7 yr
±
±
0.09b
0.17c
2.79
33.61
±
±
0.14ab 3.63a 3.76
23.04 ±
0.41 ±
3.14 ±
0.95 ±
4.08 ±
±
0.07a
0.02a
0.08a
0.18a
0.28a
0.33b
0.50c
14.99
48.61 ±
± 0.43a
3.20a
14.54
37.58 ±
0.22b ± 2.50a
2.29b
Note: Shoots include roots, stems, and branches, leaves are not included. Means for a given plant part in the same column that are followed by the same letter are not significantly different (P < 0.05).
Table 3 Cd accumulating characteristics of poplar in field sampling experiment (mean ± SD, n = 9) Stand age
Cd concentration (mg kg–1)
26
BC
TF
% Cd
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Woo
Bark
Branch
Shoot
F
extra
d
cted with NH4 NO3
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from total Cd in the soil 3 yr
5 yr
7 yr
14.95
8.43
±
±
35.00 ±
1.57a
0.85a
0.97a
13.65
9.45
±
±
27.37 ±
0.49a
0.79a
1.50b
9.07
4.84
±
±
19.03 ±
0.89b
0.39b
1.08c
24.35 ± 2.45a
28.16 ± 0.54a
15.85 ±
0.5
1.13a
5
17.28 ±
0.6
0.62a
0
1.06
1.27 5.21
15.30 ± 1.49b
9.20 ±
0.3
0.42b
2
4.37 1.01
4.09
Note: Shoots include woods, barks, and branches, leaves are not included. Values for a given plant part in the same column having the same letter are not significantly different (P < 0.05).
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