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Feasibility of phytoextraction to remediate cadmium and zinc contaminated soils
Environmental Pollution 156 (2008) 905–914
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Feasibility of phytoextraction to remediate cadmium and zinc contaminated soils G.F. Koopmans a, *, P.F.A.M. Ro¨mkens b, M.J. Fokkema b, J. Song c, Y.M. Luo c, J. Japenga b, F.J. Zhao d a
Department of Soil Quality, Wageningen University, Wageningen University and Research Centre (WUR), P.O. Box 47, 6700 AA, Wageningen, The Netherlands Alterra, WUR, P.O. Box 47, 6700 AA, Wageningen, The Netherlands c Soil and Environmental Bioremediation Research Centre, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, PR China d Soil Science Department, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK b
An experimental method is presented to be used to estimate the phytoextraction duration of a metal contaminated soil.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 February 2008 Received in revised form 8 May 2008 Accepted 12 May 2008
A Cd and Zn contaminated soil was mixed and equilibrated with an uncontaminated, but otherwise similar soil to establish a gradient in soil contamination levels. Growth of Thlaspi caerulescens (Ganges ecotype) significantly decreased the metal concentrations in soil solution. Plant uptake of Cd and Zn exceeded the decrease of the soluble metal concentrations by several orders of magnitude. Hence, desorption of metals must have occurred to maintain the soil solution concentrations. A coupled regression model was developed to describe the transfer of metals from soil to solution and plant shoots. This model was applied to estimate the phytoextraction duration required to decrease the soil Cd concentration from 10 to 0.5 mg kg1. A biomass production of 1 and 5 t dm ha1 yr1 yields a duration of 42 and 11 yr, respectively. Successful phytoextraction operations based on T. caerulescens require an increased biomass production. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Phytoextraction Cadmium Zinc Hyperaccumulator Thlaspi caerulescens Soil remediation
1. Introduction Contamination of soils with Cd and Zn is a ubiquitous problem all over the world. For example, soils in the Kempen region located in the south of The Netherlands are enriched with Cd and Zn, due to atmospheric emission of metal-bearing dust from a Zn ore smelter near the village of Budel (Fig. 1). This has resulted in a wide-spread diffuse contamination of soil affecting an area of about 350 km2 (Copius Peereboom-Stegeman and Copius Peereboom, 1989). Total Cd concentration in soil ranges from 5 to 10 mg kg1 in the immediate vicinity of this Zn ore smelter to less than 0.5 mg kg1 (background level) at a distance of 30 km. Although a total Cd concentration between 1 and 5 mg kg1 is not considered to be highly toxic, it still can cause environmental problems. Soils in the Kempen region are mostly sandy and acidic (pH < 5.5) with a low Soil Organic Matter (SOM) content (<4%). This combination of soil properties leads to a high availability of Cd and Zn in soil solution resulting in increased leaching (Degryse and Smolders, 2006) and uptake by arable crops and vegetables (Copius Peereboom-Stegeman and Copius Peereboom, 1989; Boekhold and Van der Zee,
* Corresponding author. Tel.: þ31 317 483842; fax: þ31 317 419000. E-mail address: [email protected] (G.F. Koopmans). 0269-7491/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2008.05.029
1994). Moreover, Cd and Zn levels in grass and maize from the Kempen region have been demonstrated to exceed the limit set by the European Union (EU) for animal fodder (Directive 2005/87/EC) (Rietra et al., 2004). This can, in turn, lead to increased metal levels in kidneys and liver of grazing animals beyond food quality standards of the EU (Directive 2001/466/EC) (Ro¨mkens et al., 2007). To improve conditions for grazing animals and to ultimately prevent effects on human health through food-chain accumulation, measures have to be taken to reduce transfer of Cd and Zn from soil to animal fodder. Due to the extensive size of the contaminated area in the Kempen region, use of conventional soil remediation techniques to remove metals from soil is not a feasible option. Alternatively, phytoextraction has to be considered as a measure to remediate metal contaminated soils in this region. Phytoextraction has gained world-wide attention as an environmentally friendly and potentially cost-effective technique to remove metals from soil. The use of hyperaccumulating plant species has been suggested as a promising strategy for phytoextraction (McGrath et al., 2001). Hyperaccumulators are defined as higher plants capable of accumulating >100 mg Cd kg1, >1000 mg Cu, Ni, and Pb kg1, and >10,000 mg Zn kg1 in the dry matter (dm) of shoots when growing in their natural habitats (Baker and Brooks, 1989). Many authors have proposed the use of the hyperaccumulator Thlaspi caerulescens J. & C. Presl to remediate
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pools in soil needs to be determined. Recently, a simple experimental method has been developed to achieve this goal (Japenga et al., 2007; Koopmans et al., 2007). This method involves a pot experiment in which a contaminated soil is mixed and equilibrated with an uncontaminated, but otherwise similar soil to establish a gradient in soil contamination levels reflecting the decrease, which would have been realized by phytoextraction. After one cropping cycle with the plant species of interest, regression-based log–log relationships are obtained describing the transfer of metals between the soil solid phase and soil solution as well as the accumulation of metals in plant shoots from soil solution. The coefficients of these regression models are highly soil- and plantspecific and can be implemented in a dynamic mass balance model to simulate the decrease in metal uptake with time resulting from the decrease of the sorbed metal pools in soil and to obtain a more realistic estimate of the phytoextraction duration. However, the experimental method of Japenga et al. (2007) and Koopmans et al. (2007) was only tested on a fictive soil created by spiking an uncontaminated soil with a heavily contaminated soil. The objective of our study was to test the potential of this method to predict the phytoextraction duration for a real case of soil metal contamination. For this purpose, a Cd and Zn contaminated soil from the Kempen region was used as a case study. We used the Ganges ecotype of T. caerulescens for remediation, because it can hyperaccumulate Zn just as other ecotypes, but it is far superior with respect to Cd accumulation (Lombi et al., 2000; Hutchinson et al., 2000; Assunça˜o et al., 2003a). Also, Lolium perenne L. was used, because grassland production for dairy farming is the main agricultural land use in the Kempen region. The outcome of this study can be used to facilitate the decision on whether phytoextraction is a feasible option to remediate metal contaminated soils in this region. 2. Material and methods 2.1. Soils Fig. 1. Location of the Kempen region. Contaminated soil was sampled from a nature reserve near Neerpelt in Belgium, whereas uncontaminated soil was sampled from a dairy farm near Soerendonk in The Netherlands. In the Dutch part of the Kempen region, an area of about 350 km2 is contaminated with Cd and Zn, due to emission of metal-bearing dust from a Zn ore smelter near Budel.
contaminated soils with moderate total but high available Cd and Zn concentrations (Baker et al., 1994; Brown et al., 1994; Knight et al., 1997; McGrath et al., 1997, 2006; Robinson et al., 1998; Hammer and Keller, 2003; Schwartz et al., 2003; Zhao et al., 2003; Maxted et al., 2007). However, the uncertainty of the time required to realize the desired target level in soil is one of the major constraints hampering the application of phytoextraction in practice. Long-term field experiments are not available, and estimates of the phytoextraction duration have to be based on model calculations (Maxted et al., 2007; Van Nevel et al., 2007). Removal rates of metals by plants from contaminated soils are highly dependent on soil properties, degree and bioavailability of metal contamination, and, obviously, metal uptake characteristics and biomass production of the plant species used for remediation (Lasat, 2000). Also, bioavailable metal pools in soil decrease during phytoextraction (Hammer and Keller, 2002; Keller and Hammer, 2004), which leads to a decrease of metal uptake by plants and lower metal removal rates. For example, Cd concentration in shoots of T. caerulescens decreased by a factor of 1.4 after three successive croppings on a metal contaminated soil (Keller and Hammer, 2004). Therefore, model calculations based on constant metal uptake can lead to underestimation of the phytoextraction duration. To obtain a more realistic estimate of the time required to clean up a specific contaminated soil, the response of the plant species of interest to the decrease of bioavailable metal
Soils were sampled from two sites near the Dutch–Belgian border in the Kempen region (Fig. 1). An acidic sandy soil collected from the 0 to 10 cm layer of a nature reserve near Neerpelt in Belgium was used as a source of contaminated soil. This area has been contaminated with Cd and Zn, due to atmospheric deposition of metal-bearing dust from a Belgian Zn ore smelter. The site was covered by a dense grass vegetation. An uncontaminated acidic sandy soil was collected from the 0 to 25 cm layer of a dairy farm near Soerendonk in The Netherlands. The uncontaminated site was not cultivated at the time of sampling. Distance between the two sites is about 15 km, and both soils have developed from the same parent material under similar climatological conditions. After sampling, soils were airdried, sieved through a 10-mm sieve, and stored until further use. 2.2. Pot experiments A gradient of soil metal contamination was established by mixing air-dry contaminated soil with air-dry uncontaminated soil in a ratio of 100:0, 75:25, 50:50, 25:75, and 0:100% (based on weight). After mixing, subsamples were taken from the five bulk soils for chemical analysis and for determination of the water holding capacity (WHC). The maximal WHC of these soils was on average 309 2 mL kg1 (standard deviation). Bulk soils were watered with demineralized water up to 50% of the maximal WHC, and incubated for 3 months in plastic bags at 4 C in the dark. After incubation, soils were watered with demineralized water up to 60% of the maximal WHC, which roughly equals the moisture content of these soils at field capacity, and fertilized with 30 mg N (as NH4NO3), 15 mg P (as KH2PO4), and 10 mg S (as K2SO4) kg1 soil (based on air-dry weight). Since growth rates of L. perenne and T. caerulescens (Ganges ecotype) are different, pot experiments with both plant species had separate controls consisting of uncultivated pots. For each metal contamination level, two pots were filled for L. perenne, two pots for T. caerulescens, and two pots for the control resulting in a total of 30 pots. Cone-shaped plastic pots 18 cm in height with a top diameter of 18 cm and a bottom diameter of 14 cm were used. A plastic bag with seven small needle holes at the bottom to prevent anaerobic conditions in the potted soil was placed in each pot to prevent roots from growing out of the pot. Each pot was filled with 4 kg of soil (based on air-dry weight). To prevent salt damage to germinating plant seeds, the upper 1 cm soil layer did not receive fertilizer. A PVC tube with a diameter of 3 cm and a length of 17 cm was placed vertically in the middle of each pot with the lower 3 cm part of the tube below the soil
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914 surface. This lower 3 cm part has small holes allowing for watering of the soil. Each pot was placed on an individual saucer. About 6 g seeds of L. perenne or 60 seeds of T. caerulescens were sown on the soil surface of the pots. To obtain a uniform soil cover of the latter, an additional 60 seeds were sown on bare spots after 15 d. Pot experiments were performed in a greenhouse: temperature was maintained at 18 C at night and at 20 C during the day, relative humidity varied between 30 and 60%, and a 16 h day was provided through the use of artificial light to supplement natural light at an intensity of 400 W m2. Pots were watered daily up to 60% of the maximal WHC with demineralized water and rotated to equalize exposure to light. Some leaves of T. caerulescens turned purplish with time, possibly due to P deficiency. Therefore, 8 mg P (as KH2PO4) kg1 soil (based on air-dry weight) was applied after 57 and 88 d to each pot of the experiment with T. caerulescens. After about 63 d, Thrips tabaci infested on T. caerulescens growing on one of the duplicate pots containing 100% uncontaminated soil, and an insecticide had to be used for pest control. Pot experiments were harvested after 36 d for L. perenne and after 113 d for T. caerulescens. Shoots were cut just above the soil surface. Roots of L. perenne were collected by shaking off soil. For harvesting roots of T. caerulescens, soil was air-dried, and roots were collected after sieving the soil through a 2-mm sieve. Root samples from both plant species were thoroughly washed with tap water followed by washing with demineralized water. Dry weight of the plant samples was determined after drying at 70 C for 48 h. Soil samples were dried at 40 C for 48 h and sieved through a 2-mm sieve.
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solution and sorbed metal pools. Transformation of metals in the sorbed form to more occluded forms was assumed to be negligible (De Vries et al., 2002). Leaching loss was calculated as the metal concentration in soil solution multiplied by the downward water flux from the 0 to 20 cm soil layer. We used 300 mm yr1 for the downward water flux, which is similar to the mean annual precipitation surplus in The Netherlands. Atmospheric deposition was set at 0.2 g Cd and 27.7 g Zn ha1 yr1 (Delahaye et al., 2003). The dynamic mass balance model was applied to estimate the phytoextraction duration of the 100% contaminated soil. Metal contamination was assumed to occur only in the 0–20 cm soil layer, which is similar to the shallow active rooting zone of T. caerulescens (Keller et al., 2003). We used 1.4 kg L1 for soil density. Biomass production of plants in pot experiments is often much higher than the production under field conditions (Delorme et al., 2000). Therefore, we used field data for the biomass production of L. perenne and T. caerulescens. Biomass production of permanent grassland in dairy farming on sandy soils in The Netherlands varies between 8 and 14 t dm ha1 yr1 (Vellinga and Andre´, 1999). In our model calculations, biomass production of L. perenne was set at these two outer values. Biomass production of T. caerulescens was set at 1 t dm ha1 yr1 (Robinson et al., 1998; Hammer and Keller, 2003; Keller et al., 2003; McGrath et al., 2006), whereas a value of 5 t dm ha1 yr1 was used to show the effect of an increased production on the phytoextraction duration.
3. Results and discussion
2.3. Chemical analyses
3.1. Soil properties Soil organic matter, reactive Al and Fe oxides, clay (<2 mm), unbuffered Cation Exchange Capacity (CEC), and total extractable metal concentrations of the five soils used for the pot experiments were determined using standard analytical procedures (Houba et al., 1997): SOM was determined by loss-on-ignition at 550 C, clay by the sieve and pipette method, reactive metal oxides by extraction with a mixture of ammonium oxalate and oxalic acid, CEC by the unbuffered 0.01 M BaCl2 method, and total extractable metal concentrations by digestion with aqua regia. Metal concentrations were measured with an Inductively Coupled Plasma-Atomic Emission Spectrometer (ICP-AES). Metals extractable with 0.43 M HNO3 (Houba et al., 1997) and pH and concentrations of Dissolved Organic Carbon (DOC) and metals in 1:10 (w/v) 0.01 M CaCl2 extracts (Houba et al., 2000) were determined before and after the pot experiments. The pH was measured with a combined glass-electrode, DOC with a fully automated segmented flow analyser (Skalar, SK12) by persulphate and tetraborate oxidation under ultraviolet light and infrared detection, and metal concentrations in the 0.43 M HNO3 and 0.01 M CaCl2 extracts with an ICP-AES and ICP-Mass Spectrometer (ICP-MS), respectively. Except for clay, all soil analyses were performed in duplicate. Dried plant shoots and roots were ground in a titanium grinder. Plant material was digested by microwave destruction (Novozamsky et al., 1996). Metal concentrations in the digests were measured with an ICP-MS. Quality of the analyses was monitored by including blanks and soil and plant standards in each batch and an interlaboratory exchange program. 2.4. Statistics Linear regression analyses were performed to derive models describing the transfer of metals between the soil solid phase and soil solution as well as the accumulation of metals in plant shoots from soil solution. For the sorbed metal pools in soil, results of the 0.43 M HNO3 extraction method were used. Metals extracted with HNO3 are considered as estimates of sorbed metals reacting with binding sites located on the surfaces of SOM, reactive metal oxides, and clay, and they control the metal concentrations in soil solution, whereas metals extracted with aqua regia include the more occluded forms (Weng et al., 2001; Tipping et al., 2003). Metal concentrations in the 0.01 M CaCl2 extracts were used as an estimate for metals in soil solution (Degryse et al., 2003). Metal concentrations in the soil solution extracts were determined before and after the pot experiments, whereas plant shoot metal concentrations were determined only at the end. Metal accumulation in plant shoots, however, is a reflection of the metal concentrations in soil solution occurring throughout the entire growth period. Therefore, plant shoot metal concentrations were compared to the mean of the metal concentrations in the soil solution extracts before and after the pot experiments. Duplicate pots were treated as individual samples. All data were log-transformed. Significance of R2adj and predictor variables was assessed using F-tests and t-tests, respectively. Least significant difference method with a 0.05 probability value was used to determine effects of (i) soil contamination level on shoot and root biomass and (ii) treatment (control versus planted pots) on sorbed metal pools and on pH and concentrations of DOC and metals in the soil solution extracts. Statistical analyses were performed with Genstat, Release 9.2. 2.5. Phytoextraction duration The regression models were implemented in a dynamic mass balance model similar to the approach used by De Vries et al. (2002). Changes in the sorbed metal pools in soil with time were predicted by adding input through atmospheric deposition and by subtracting outputs through leaching and plant uptake. During phytoextraction, equilibrium was assumed between metal concentrations in soil
Properties of the 100% uncontaminated soil used to dilute the 100% contaminated soil need to be as similar as possible to those of the latter so as to avoid changes in the solubility of metals after mixing (Japenga et al., 2007; Koopmans et al., 2007). In Table 1, selected properties of the five soils used for the pot experiments are presented. Differences in pH, SOM, the sum of reactive Al and Fe oxides ([Al þ Fe]ox), clay, CEC, and DOC between the 100% contaminated soil and the 100% uncontaminated soil were small in comparison with the high variability normally found for these soil properties in acidic sandy soils (Koopmans et al., 2006). Mixing caused pH to decrease gradually from 5.4 in the 100% contaminated soil to 5.1 in the 100% uncontaminated soil, SOM from 3.8 to 3.2%, [Al þ Fe]ox from 84.0 to 56.4 mmol kg1, and CEC from 52.3 to 41.3 mmol kg1, whereas DOC increased from 5.5 to 9.4 mg L1. Total metal concentrations in the 100% contaminated soil were 19 (Cd) and 13 (Zn) times greater than the Dutch target values of 0.5 mg Cd and 60 mg Zn kg1 soil. In the 100% uncontaminated soil, the total Zn concentration was lower than the Dutch target value, whereas total Cd was the same as the target value. Sorbed metal pools accounted for on average 94% (Cd) and 78% (Zn) of the total metal concentrations. Hence, most of the total metal concentrations can exchange with soil solution and can become available with time for plant uptake. 3.2. Plant growth and metal concentrations Shoot biomass of L. perenne was constant for most soils, but decreased significantly for the 100% contaminated soil (Table 2). This may be due to metal phytotoxicity, because L. perenne grown on this soil had clearly visible chlorosis symptoms. In contrast, shoot biomass of T. caerulescens grown on the 100% uncontaminated soil decreased significantly compared to the other soils (Table 2). This may, in part, be explained by infestation with T. tabaci of T. caerulescens grown on one of the duplicate pots containing this soil leading to a premature senescence of leaves. T. caerulescens grown on this pot was possibly more susceptible to thrips, because shoots of these plants contained much less Cd than those of the plants grown on the other soils (Table 2). Hyperaccumulation of Cd can protect T. caerulescens from leaf feeding damage by thrips (Jiang et al., 2005). Metal concentrations in shoots of T. caerulescens were between 165 and 279 (Cd) and between 5 and 51 (Zn) times higher than those in shoots of L. perenne (Table 2), emphasizing the great ability of T. caerulescens to take up and translocate these metals from roots
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Table 1 Soil properties of the contaminated soil and uncontaminated soil and intermediate soil mixtures before the start of the pot experiments Contaminated soil (%)
100 75 50 25 0
pHa
SOMb (%)
5.4 0.03 5.3 0.01 5.3 0.01 5.2 0.00 5.1 0.01
3.8 0.0 3.7 0.2 3.5 0.1 3.3 0.1 3.2 0.1
[Al þ Fe]oxc (mmol kg1)
Clay (%)
84.0 1.2 79.5 0.4 72.7 1.2 66.1 0.6 56.4 1.0
2 3 2 2 2
CECd (mmol kg1)
52.3 0.5 54.6 0.6 53.3 1.6 47.4 0.6 41.3 1.3
DOCa (mg L1)
5.5 0.2 6.7 0.1 8.1 0.7 9.3 0.6 9.4 0.1
Dissolved metal concentrationa
Sorbed metal concentratione
Total metal concentrationf
Cd (mg L1)
Zn (mg L1)
Cd (mg kg1)
Zn (mg kg1)
Cd (mg kg1)
Zn (mg kg1)
201 6 162 2 120 1 62.6 0.2 8.4 0.5
13.7 0.4 10.6 0.2 7.7 0.0 4.0 0.0 0.32 0.03
10.2 0.4 7.9 0.4 5.0 0.3 2.7 0.2 0.45 0.02
689 26 516 25 379 28 181 18 16.1 0.8
9.8 0.6 8.5 0.4 5.6 0.0 3.0 0.1 0.51 0.03
776 43 660 29 423 4 212 2 33.3 1.4
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
Values represent mean standard deviation of the duplicate analyses. a Measured in 0.01 M CaCl2 extracts. b Soil Organic Matter (SOM). c Reactive Al and Fe oxides extracted with a mixture of ammonium oxalate and oxalic acid ([Al þ Fe]ox). d Unbuffered Cation Exchange Capacity (CEC). e Sorbed metal concentrations extracted with 0.43 M HNO3. f Total extractable soil metal concentrations determined by digestion with aqua regia.
Table 2 Biomasss production of shoot and roots, shoot and root Cd and Zn concentrations, and Cd and Zn shoot:root ratios of L. perenne and T. caerulescens Contaminated soil (%)
100 75 50 25 0
L. perenne
T. caerulescens
Shoots (g pot1)
Roots (g pot1)
11.2 0.1a 13.7 0.6b 13.7 0.4b 14.2 0.4b 13.5 0.3b
6.7 0.3a 7.1 0.1a 7.2 0.7a 10.4 3.3a 8.9 1.1a
Shoots
Roots
Shoot:root ratio
Cd (mg kg1)
Zn (mg kg1)
Cd (mg kg1)
Zn (mg kg1)
Cd
Zn
3.5 0.1 2.7 0.2 2.0 0.1 1.2 0.1 0.27 0.03
824 9 621 7 470 6 245 2 40.7 2.6
47.9 0.1 33.3 1.0 22.7 1.2 15.3 0.4 3.7 0.3
3734 28 2342 56 1638 2 944 23 175 4
0.07 0.00 0.08 0.01 0.09 0.01 0.08 0.01 0.07 0.00
0.22 0.00 0.27 0.01 0.29 0.00 0.26 0.00 0.23 0.01
Shoots (g pot1)
Roots (g pot1)
15.6 0.0a 15.6 0.1a 15.5 2.0a 15.7 0.6a 10.8 2.0b
4.3 0.0ab 4.6 0.2a 5.3 0.3a 4.1 0.5ab 3.1 1.2b
Shoots
Roots
Shoot:root ratio
Cd (mg kg1)
Zn (mg kg1)
Cd (mg kg1)
Zn (mg kg1)
Cd
Zn
749 73 694 0 561 81 270 23 43.9 7.8
4044 400 4321 357 4264 341 3776 60 2081 105
375 1 349 12 269 13 272 54 92.4 0.7
1441 21 1228 15 1177 43 895 85 389 123
2.0 0.2 2.0 0.1 2.1 0.2 1.0 0.1 0.48 0.09
2.8 0.2 3.5 0.3 3.6 0.4 4.2 0.5 5.6 1.5
Means of biomasss production of shoot and roots for L. perenne and T. caerulescens within 1 column followed by different letters are significantly different at the P < 0.05 level. Values represent mean standard deviation of the duplicate pots.
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
to shoots. Metal concentrations in shoots of L. perenne were much smaller than those in roots. Consequently, shoot:root ratios of Cd and Zn were far below 1 for this plant species (Table 2), which is typical for nonhyperaccumulating plants (McGrath et al., 2001). In contrast to L. perenne, metal concentrations in shoots of T. caerulescens were much greater than those in roots. The shoot:root ratio of Cd was above 1 for most soils (Table 2). Hyperaccumulating plant species usually have a shoot:root ratio above 1 (McGrath et al., 2001). For most soils, the Cd concentration in shoots of T. caerulescens by far exceeded the hyperaccumulation level of 100 mg kg1 (Table 2), as defined by Baker and Brooks (1989). This Cd hyperaccumulation trait is typical for the Ganges ecotype (Lombi et al., 2000; Hutchinson et al., 2000). The shoot:root ratio of Zn was above 1 for all soils, although the Zn concentration in shoots
A
12
L. perenne Control
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of T. caerulescens did not reach the hyperaccumulation level of 10,000 mg kg1 dm (Table 2) (Baker and Brooks, 1989). 3.3. Metal pools Growth of L. perenne hardly changed the sorbed metal pools, whereas the sorbed Cd pool decreased significantly for most soils after one cropping of T. caerulescens (Fig. 2). The extent of this reduction varied between 43 and 57% emphasizing the great ability of the Ganges ecotype to remove Cd from soil. Three successive croppings of a Cd hyperaccumulating ecotype of T. caerulescens on a metal contaminated acidic soil resulted in a similar reduction of 59% of the 2 M HNO3-extractable Cd pool in a pot experiment of Keller and Hammer (2004). The sorbed Zn pool decreased by 7–52%
B
12
T. caerulescens
a
Control
a a 10
a
a a
8
6
Sorbed Cd (mg kg-1)
Sorbed Cd (mg kg-1)
10
a a
4
8 b 6
a b
4
a a b 2
a
2
b
a a 0
100
75
50
25
a a 0
0
100
C
800
L. perenne
D
50
800
25
0
T. caerulescens
a
Control
a b
75
Contaminated soil (%)
Contaminated soil (%)
Control
b
600
600 a a
Sorbed Zn (mg kg-1)
Sorbed Zn (mg kg-1)
a b
a a
400
a a
200
400
a a
a a
200
a a
a a 0
100
75
50
25
Contaminated soil (%)
0
0
100
75
50
25
0
Contaminated soil (%)
Fig. 2. Sorbed Cd (A and B) and Zn pools (C and D) in the soil samples taken after the pot experiments with L. perenne (A and C) and T. caerulescens (B and D). Values of the control represent mean standard deviation of the duplicate analyses, whereas values of the planted pots represent mean standard deviation of the duplicate pots. Means with different letters are significantly different at the P < 0.05 level.
12.5 0.9b 10.6 0.1b 6.9 0.0b 3.2 0.0a 0.11 0.03a Values of the control pots represent mean standard deviation of the duplicate analyses, whereas values for the planted pots represent mean standard deviation of the duplicate pots. Means of pH, DOC, and total dissolved Cd and Zn concentrations for L. perenne and T. caerulescens within one row followed by different letters are significantly different at the P < 0.05 level.
14.1 0.6a 12.1 0.0a 9.1 0.6a 4.4 0.1a 0.40 0.00a
Control Plant
98.7 1.2b 69.7 2.4b 41.1 1.7b 20.6 1.9b 2.8 0.5b 200 9a 169 1a 128 6a 66.0 0.8a 9.5 0.1a
Control Plant
7.8 0.1b 10.1 0.1b 9.9 0.2b 9.8 1.0b 9.9 0.4a 5.1 0.6a 7.5 0.0a 6.9 0.3a 6.9 0.0a 11.3 0.7a
Control Plant
5.4 0.01b 5.2 0.03a 5.1 0.00b 5.1 0.01b 5.0 0.00b 5.3 0.01a 5.2 0.03a 5.1 0.01a 5.0 0.00a 4.8 0.02a
Control Plant
14.4 0.3b 11.1 0.0a 8.1 0.2a 4.2 0.1a 0.34 0.00a 15.0 0.1a 11.4 0.3a 8.3 0.0a 4.4 0.1a 0.33 0.00a
Control Plant
211 1b 169 0a 122 3a 65.3 1.0a 8.8 0.1a 217 0a 174 4a 126 1a 66.7 0.8a 8.5 0.1a
Control Plant
4.7 0.1a 6.2 0.4a 7.2 0.0a 8.9 0.5a 9.2 0.0a 4.9 0.3a 6.5 0.0a 7.7 0.3a 9.1 0.2a 8.8 0.3a
Control
5.4 0.01a 5.3 0.01a 5.2 0.04a 5.1 0.00a 4.9 0.01a
Plant Control
5.3 0.04a 5.3 0.01a 5.2 0.00a 5.1 0.01a 5.0 0.00a 100 75 50 25 0
Zn (mg L1) Cd (mg L1) DOC (mg L1) pH
T. caerulescens
Zn (mg L1) Cd (mg L1) DOC (mg L1) pH
Metal concentrations in the soil solution extracts could be very well predicted from the sorbed metal pools with R2adj values of 98.7% (Cd) and 99.3% (Zn) (Fig. 3). Although pH and other soil properties (SOM and Alox) contributed significantly to the regression models of Cd and Zn, R2adj only slightly further improved by including these soil properties (not shown). Obviously, pH has to be included when comparing soils with a wide pH range (Sauve´ et al., 2000; Tipping et al., 2003). In our experimental set-up, however, differences in pH as well as in other soil properties were deliberately minimized so as to avoid changes in metal solubility after mixing the 100% contaminated soil with the 100% uncontaminated soil. The sum of the metal uptake in the shoots and roots of T. caerulescens was 2.8–3.3 (Cd) and 0.8–2.0 (Zn) times greater than the decrease of the metal concentrations in the soil solution extracts (not shown). Hence, replenishment of Cd and Zn in the soil solution extracts must have occurred through the release of metals bound to the soil solid phase. Replenishment of bioavailable metal pools during cropping of T. caerulescens on metal contaminated soils has been reported previously (Knight et al., 1997; Whiting et al., 2001; Hammer and Keller, 2002; Keller and Hammer, 2004). This gives rise to the question whether a new equilibrium has been established between metal concentrations in the soil solution extracts and metals bound to the soil solid phase after one cropping of
L. perenne
3.4. Regression models
Contaminated soil (%)
after one cropping of T. caerulescens, although this reduction was only significant for the 100% contaminated soil (Fig. 2). The sum of the Cd uptake in the shoots and roots of T. caerulescens accounted for 74 to 89% of the decrease of the sorbed Cd pool (not shown). However, the Cd concentration measured in roots may overestimate the amount of Cd actually taken up by roots, because Cd in roots of T. caerulescens not only includes Cd in the root symplast, but also Cd bound in the apoplast (Zhao et al., 2002). Growth of L. perenne hardly affected the composition of the soil solution extracts, whereas metal concentrations decreased significantly for most soils after one cropping of T. caerulescens (Table 3). The extent of this reduction varied between 51 and 71% for Cd and between 12 and 72% for Zn. Hence, T. caerulescens seems to have potential to reduce the readily bioavailable metal pools in soil, a concept referred to as Bioavailable Contaminant Stripping (BCS) (Hamon and McLaughlin, 1999). The purpose of BCS is to reduce environmental risks posed by the presence of metals in soil through decreasing the readily bioavailable metal pools within a limited number of croppings instead of decreasing the total metal concentrations. For an environmentally safe application, kinetics of metal replenishment in soil solution after BCS has been applied need to be understood. Release of metals from the soil solid phase can increase the environmental risks again in case of a disequilibrium between metal concentrations in soil solution and metals bound to the soil solid phase. This issue will be discussed in more detail in the next paragraph. Growth of T. caerulescens resulted in small, but significant increases in pH and DOC for most soils (Table 3). Apparently, the ability of this plant species to remove metals from our soils was not related to rhizosphere acidification, which is in agreement with previous studies (Knight et al., 1997; McGrath et al., 1997; Hutchinson et al., 2000; Schwartz et al., 2003). Increase of DOC may be due to the release of root exudates by T. caerulescens, but this mechanism is known not to be involved in the metal hyperaccumulation behavior of the Ganges ecotype (Zhao et al., 2001). Hyperaccumulation of metals by T. caerulescens is likely to involve multiple traits, with enhanced metal uptake, root to shoot translocation, and vacuolar sequestration in leaf cells at least being partly under genetic control (Assunça˜o et al., 2003b).
Plant
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
Table 3 The pH and DOC and Cd and Zn concentrations in the 0.01 M CaCl2 extracts obtained from the soil samples of the pot experiments with L. perenne and T. caerulescens
910
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A
B
2.5
4.5
4.0
1.5 Initial soils Control L. perenne Control T. caerulescens
1.0
log y = 1.29 ± 0.01*** + (1.06 ± 0.02*** log x)
0.5
R
0.0 -1.0
-0.5
0.0
2 adj
Log dissolved Zn (µg L-1)
2.0
Log dissolved Cd (µg L-1)
911
= 98.7%*** (n = 35)
0.5
1.0
Log sorbed Cd (mg
3.5
Initial soils Control L. perenne Control T. caerulescens
3.0
2.5
log y = 1.29 ± 0.03*** + (1.02 ± 0.01*** log x) 2 R adj = 99.3%*** (n = 35)
2.0
1.5 0.5
1.5
kg-1)
1.0
1.5
2.0
2.5
3.0
Log sorbed Zn (mg kg-1)
Fig. 3. Cadmium (A) and Zn concentrations (B) in the 1:10 (w/v) 0.01 M CaCl2 extracts plotted against the sorbed metal pools with the regression model describing the soil solid phase–soil solution relationship (regression coefficients standard error). For the regression analysis, all soil samples were used including those taken before and after the pot experiments with L. perenne and T. caerulescens. Statistical significance: ***for P < 0.001.
T. caerulescens. Metal concentrations in the soil solution extracts seemed to be close to equilibrium with the sorbed metal pools, because partitioning of Cd and Zn between the solid phase of the bulk soil and soil solution could be described with a single regression model for all soil samples including those taken before and after the pot experiments with L. perenne and T. caerulescens (Fig. 3). Apparently, plant uptake of Cd and Zn was followed by instantaneous release of these metals from the soil solid phase and was not kinetically limited by desorption of these metals. This finding supports our assumption of equilibrium between metal concentrations in soil solution and sorbed metal pools as used in the dynamic mass balance model calculations to predict the phytoextraction duration. However, a local disequilibrium in the rhizosphere resulting from the sink effect induced by roots of T. caerulescens would not have been detected, because we mixed our soil samples before chemical analysis. Our hypothesis of an apparent equilibrium is supported by measurement of Cd and Zn desorption kinetics in soils with the technique of diffusive gradients in thin-
A
3.5
films (Ernstberger et al., 2005). In these experiments, desorption of Cd and Zn from the soil solid phase was not kinetically limited. Analogous to our finding, the inorganic P concentration in 0.01 M CaCl2 extracts of soil samples taken at various stages of a long-term pot experiment in which a highly P-enriched soil was remediated by 31 successive croppings of L. perenne was continuously in equilibrium with the sorbed P pool (Koopmans et al., 2004). The question whether equilibrium has indeed been reached in our pot experiments requires more investigation, but this falls outside the scope of this study. Hence, application of BCS to contaminated soils in the Kempen region may result in a stable decrease of the metal concentrations in soil solution with time. However, lack of legislative support hampers the application of BCS in practice, because legislation on soil remediation is still based on target values using total soil metal concentrations instead of chemically available pools (Keller and Hammer, 2004). Metal accumulation in plant shoots could be very well predicted from the metal concentrations in the soil solution extracts
B
4.0
3.0
2.0 1.5
log y = 0.98 ± 0.06*** + (0.89 ± 0.04*** log x) 2
R
adj
= 98.6%*** (n = 10)
1.0 L. perenne T. caerulescens
0.5 0.0
Log Zn shoots (mg kg-1)
Log Cd shoots (mg kg-1)
3.5 2.5
log y = 2.91 ± 0.07*** + (0.18 ± 0.02*** log x) 2
R
3.0
-1.0 0.5
L. perenne T. caerulescens
2.0
log y = -0.41 ± 0.08** + (0.79 ± 0.02*** log x) R
log y = -1.33 ± 0.04*** + (0.80 ± 0.02*** log x) R2adj = 99.3%*** (n = 10)
1.0
1.5
2.0
2.5
Log dissolved Cd (µg L-1)
91.3%*** (n = 10)
2.5
1.5 -0.5
adj=
1.0 2.0
2.5
3.0
2 adj
3.5
= 99.3%*** (n = 10)
4.0
4.5
Log dissolved Zn (µg L-1)
Fig. 4. Cadmium (A) and Zn concentrations (B) in the shoots of L. perenne and T. caerulescens plotted against metal concentrations in the 1:10 (w/v) 0.01 M CaCl2 extracts with the regression model describing the soil solution–plant relationship (regression coefficients standard error). Statistical significance: **for P < 0.01 and ***for P < 0.001.
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Table 4 Predicted phytoextraction duration to reach the Dutch target values (total metal concentrations of 0.5 mg Cd kg1 and 60 mg Zn kg1) in the 0–20 cm layer of the 100% contaminated soil from the Kempen region (Fig. 1) using L. perenne and T. caerulescens for remediation Metal
L. perenne 8 t ha (yr)
Cd Zn
128 91
1
yr
T. caerulescens 1
1
14 t ha (yr)
yr
1
124 82
1 t ha1 yr1 (yr)
5 t ha1 yr1 (yr)
42 82
11 45
Biomass production of L. perenne and T. caerulescens was set at 8 and 14 t ha1 yr1 and 1 and 5 t ha1 yr1, respectively.
with R2adj values of 99.3% (Cd and Zn) for L. perenne and 98.6% (Cd) and 91.3% (Zn) for T. caerulescens (Fig. 4). Accumulation of Cd in the shoots of L. perenne and T. caerulescens clearly increased with the dissolved Cd concentration. For Zn, L. perenne showed the same behavior, but the behavior of T. caerulescens was different. Accumulation of Zn in the shoots of T. caerulescens depended much less on the Zn concentration in the soil solution extracts. Enabled by a high-affinity Zn uptake mechanism in the roots, T. caerulescens is able to accumulate large amounts of Zn at a relatively constant rate from the solution phase over a wide range of Zn concentrations (Pence et al., 2000). This behavior is typical for Zn hyperaccumulating plant species, and the ability of different T. caerulescens ecotypes to hyperaccumulate Zn has been reported many times before (Hutchinson et al., 2000; Lombi et al., 2000; Assunça˜o et al., 2003a). 3.5. Phytoextraction duration The time required to realize the target value in the 0–20 cm layer of the 100% contaminated soil using a biomass production of 5 t dm ha1 yr1 for T. caerulescens was 11 yr for Cd, whereas 45 yr would be needed to clean up the Zn contamination (Table 4 and Fig. 5). Apparently, phytoextraction is more likely to be feasible for Cd than for Zn, which has been concluded previously (McGrath et al., 1997, 2006; Robinson et al., 1998; Hammer and Keller, 2003; Schwartz et al., 2003; Zhao et al., 2003). A biomass production of
A 11
5 t dm ha1 yr1 for T. caerulescens, however, is unrealistically high, because the production of this plant species in field experiments has been reported to vary around 1–2 t dm ha1 yr1 (Robinson et al., 1998; Hammer and Keller, 2003; Keller et al., 2003; McGrath et al., 2006). The phytoextraction duration for the 100% contaminated soil increased to 42 yr for Cd and to 82 yr for Zn using a biomass production of 1 t dm ha1 yr1 for T. caerulescens, whereas the phytoextraction duration using L. perenne for remediation was (much) longer (Table 4). Moreover, we estimated the phytoextraction duration for soils with a lower initial sorbed Cd concentration, which are located at further distance from the Zn ore smelter, using T. caerulescens for remediation and a biomass production of 1 t dm ha1 yr1. Phytoextraction duration decreased from 42 yr for a soil with 10.2 mg Cd kg1 to 10 yr for a soil with 1 mg Cd kg1 (Fig. 6). Since any phytoextraction duration exceeding 10 yr would be totally uneconomic (Robinson et al., 1998), phytoextraction does not seem to be a feasible option for the remediation of metal contaminated soils in the Kempen region at present. Hence, the technique of phytoextraction clearly needs to be improved before it is ready for application in practice (Van Nevel et al., 2007). The major constraint, which seems to reduce the phytoextraction effectiveness of T. caerulescens, is the low biomass production of this plant species under field conditions. The biomass production of T. caerulescens can be increased with improved knowledge of agricultural management practices and screening and plant breeding (Zhao et al., 2003). For example, N fertilizer application increased the biomass production of this plant species resulting in greater metal removal rates (Schwartz et al., 2003). Fertilizing crops of T. caerulescens grown in base-mine tailings increased biomass production by a factor of 2–3 without significant reductions of shoot metal concentrations (Bennett et al., 1998). A biomass production of 5 t dm ha1 yr1, therefore, may be achievable for T. caerulescens (Zhao et al., 2003). Using this biomass production, phytoextraction duration decreased from 11 yr for a soil with 10.2 mg Cd kg1 to 3 yr for a soil with 1 mg Cd kg1 (Fig. 6). Hence, phytoextraction using T. caerulescens holds promise to remediate contaminated soils with moderate total Cd concentrations in the future, but improvement of this technique by increasing the biomass production of this plant species is a prerequisite.
B
10
800 700 600
8
Sorbed Zn (mg kg-1)
Sorbed Cd (mg kg-1)
9
7 6 5 4 3
400 300 1 t dm ha-1 yr-1
200
2
1 t dm ha-1 yr-1
100
1 0
500
5 t dm ha-1 yr-1
0
10
20
30
40
Time (yr)
50
60
70
0
Target value
5 t dm ha-1 yr-1
Target value
0
20
40
60
80
100
120
Time (yr)
Fig. 5. Modelled decrease of the sorbed Cd (A) and Zn pools (B) in the 0–20 cm layer of the 100% contaminated soil from the Kempen region (Fig. 1) with time, predicted by calculating the metal concentrations in the shoots of T. caerulescens and leaching as a log-linear function of the metal concentrations in the soil solution extracts (Fig. 4). Partitioning of metals between soil solid phase and soil solution was calculated using the regression models presented in Fig. 3. A biomass production of 1 and 5 t dm ha1 yr1 was used in the model calculations. Number of harvests required to complete phytoextraction can be read from the x-axis of the figure as the number of years assuming one annual harvest.
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
50
40
-1
-1
Phytoextraction duration (yr)
1 t dm ha yr
30
20
-1
5 t dm ha yr
-1
10
0
1
2
3
4
5
6
7
8
9
10
11
Initial sorbed Cd pool (mg kg-1) Fig. 6. Time required to remediate the 0–20 cm layer of soils from the Kempen region (Fig. 1) as a function of the initial sorbed Cd pool in soil, predicted by calculating the metal concentrations in the shoots of T. caerulescens and leaching as a log-linear function of the metal concentrations in soil solution (Fig. 4). Partitioning of Cd between the soil solid phase and soil solution was calculated using the regression model presented in Fig. 3. A biomass production of 1 and 5 t dm ha1 yr1 was used in the model calculations.
Acknowledgements The authors kindly acknowledge Erik Smolders and Fien Degryse and the Beheersteam Hageven for help in selecting and locating the contaminated soil in the nature reserve het Hageven. This project was financed by the Chinese Ministry of Science and Technology (contract no. 2006DFA91940 and 2004CB720403) and the Royal Dutch Academy of Sciences (contract no. 04-PSA-E-05). Rothamsted Research receives grant-aided support from the UK Biotechnology and Biological Sciences Research Council.
References Assunça˜o, A.G.L., Bookum, W.M., Nelissen, H.J.M., Vooijs, R., Schat, H., Ernst, W.H.O., 2003a. Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytologist 159, 411–419. Assunça˜o, A.G.L., Schat, H., Aarts, M.G.M., 2003b. Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytologist 159, 351–360. Baker, A.J.M., Brooks, R.R., 1989. Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126. Baker, A.J.M., McGrath, S.P., Sidoli, C.M.D., Reeves, R.D., 1994. The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resources, Conservation and Recycling 11, 41–49. Bennett, F.A., Tyler, E.K., Brooks, R.R., Gregg, P.E.H., Stewart, R.B., 1998. Fertilisation of hyperaccumulators to enhance their potential for phytoremediation and phytomining. In: Brooks, R.R. (Ed.), Plants that Hyperaccumulate Heavy Metals. CAB International, Wallingford, UK, pp. 249–259. Boekhold, A.E., Van der Zee, S.E.A.T.M., 1994. Field scale variability of cadmium and zinc in soil and barley. Environmental Monitoring and Assessment 29, 1–15. Brown, S.L., Chaney, R.L., Angle, J.S., Baker, A.J.M., 1994. Phytoremediation potential of Thlaspi caerulescens and bladder campion for zinc- and cadmiumcontaminated soil. Journal of Environmental Quality 23, 1151–1157. Copius Peereboom-Stegeman, J.H.J., Copius Peereboom, J.W., 1989. The intake of cadmium in the Kempen, an area in the south of the Netherlands. Ecotoxicology and Environmental Safety 18, 93–108.
913
Degryse, F., Broos, K., Smolders, E., Merckx, R., 2003. Soil solution concentration of Cd and Zn can be predicted with a CaCl2 soil extract. European Journal of Soil Science 54, 149–157. Degryse, F., Smolders, E., 2006. Mobility of Cd and Zn in polluted and unpolluted Spodosols. European Journal of Soil Science 57, 122–133. Delahaye, R., Fong, P.K.N., Van Eerdt, M.M., Van der Hoek, K.W., Olsthoorn, C.S.M., 2003. Emission of Seven Heavy Metals to Agricultural Land. Centraal Bureau voor de Statistiek, Voorburg, The Netherlands (in Dutch). Delorme, T.A., Angle, J.S., Coale, F.J., Chaney, R.L., 2000. Phytoremediation of phosphorus-enriched soils. International Journal of Phytoremediation 2, 173–181. De Vries, W., Ro¨mkens, P.F.A.M., Van Leeuwen, T., Bronswijk, J.J.B., 2002. Heavy metals. In: Haygarth, P.M., Jarvis, S.C. (Eds.), Agriculture, Hydrology and Water Quality. CAB International, Wallingford, pp. 107–132. Ernstberger, H., Zhang, H., Tye, A., Young, S., Davison, W., 2005. Desorption kinetics of Cd, Zn, and Ni measured in soils by DGT. Environmental Science & Technology 39, 1591–1597. Hammer, D., Keller, C., 2002. Changes in the rhizosphere of metal-accumulating plants evidenced by chemical extractants. Journal of Environmental Quality 31, 1561–1569. Hammer, D., Keller, C., 2003. Phytoextraction of Cd and Zn with Thlaspi caerulescens in field trials. Soil Use and Management 19, 144–149. Hamon, R.E., McLaughlin, M.J., 1999. Use of the hyperaccumulator Thlaspi caerulescens for bioavailable contaminent stripping. In: Wenzel, W.W., Adriano, D.C., Alloway, B., Doner, H., Keller, C., Lepp, N.W., Mench, M., Naidu, R., Pierzynski, G. M. (Eds.), Proceedings of the Fifth International Conference on the Biogeochemistry of Trace Elements (ICOBTE), 12–15 July, 1999, Vienna, Austria, pp. 908–909. Houba, V.J.G., Temminghoff, E.J.M., Gaikhorst, G.A., Van Vark, W., 2000. Soil analysis procedures using 0.01 M calcium chloride as extraction reagent. Communications in Soil Science and Plant Analysis 31, 1299–1396. Houba, V.J.G., Van der Lee, J.J.G., Novozamsky, I., 1997. Soil and Plant Analysis. Part 1: Soil Analysis Procedures. Wageningen University, Wageningen, The Netherlands. Hutchinson, J.J., Young, S.D., McGrath, S.P., West, H.M., Black, C.R., Baker, A.J.M., 2000. Determining uptake of ‘non-labile’ soil cadmium by Thlaspi caerulescens using isotopic dilution techniques. New Phytologist 146, 453–460. Japenga, J., Koopmans, G.F., Song, J., Ro¨mkens, P.F.A.M., 2007. A feasibility test to estimate the duration of phytoextraction of heavy metals from polluted soils. International Journal of Phytoremediation 9, 115–132. Jiang, R.F., Ma, D.Y., Zhao, F.J., McGrath, S.P., 2005. Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytologist 167, 805–814. Keller, C., Hammer, D., 2004. Metal availability and soil toxicity after repeated croppings of Thlaspi caerulescens in metal contaminated soils. Environmental Pollution 131, 243–254. Keller, C., Hammer, D., Kayser, A., Richner, W., Brodbeck, M., Sennhauser, M., 2003. Root development and heavy metal phytoextraction efficiency: comparison of different plant species in the field. Plant and Soil 249, 67–81. Knight, B., Zhao, F.J., McGrath, S.P., Shen, Z.G., 1997. Zinc and cadmium uptake by the hyperaccumulator Thlaspi caerulescens in contaminated soils and its effects on the concentration and chemical speciation of metals in soil solution. Plant and Soil 197, 71–78. Koopmans, G.F., Chardon, W.J., Dekker, P.H.M., Ro¨mkens, P.F.A.M., Schoumans, O.F., 2006. Comparing different extraction methods for estimating phosphorus solubility in various soil types. Soil Science 171, 103–116. Koopmans, G.F., Chardon, W.J., Ehlert, P.A.I., Dolfing, J., Suurs, R.A.A., Oenema, O., Van Riemsdijk, W.H., 2004. Phosphorus availability for plant uptake in a phosphorus-enriched noncalcareous sandy soil. Journal of Environmental Quality 33, 965–975. Koopmans, G.F., Ro¨mkens, P.F.A.M., Song, J., Temminghoff, E.J.M., Japenga, J., 2007. Predicting the phytoextraction duration to remediate heavy metal contaminated soils. Water, Air and Soil Pollution 181, 355–371. Lasat, M.M., 2000. Phytoextraction of metals from contaminated soil: a review of plant/soil/metal interaction and assessment of pertinent agronomic issues. Journal of Hazardous Substance Research 2, 1–25. Lombi, E., Zhao, F.J., Dunham, S.J., McGrath, S.P., 2000. Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytologist 145, 11–20. Maxted, A.P., Black, C.R., West, H.M., Crout, N.M.J., McGrath, S.P., Young, S.D., 2007. Phytoextraction of cadmium and zinc from arable soils amended with sewage sludge using Thlaspi caerulescens: development of a predictive model. Environmental Pollution 150, 363–372. McGrath, S.P., Lombi, E., Gray, C.W., Caille, N., Dunham, S.J., Zhao, F.J., 2006. Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environmental Pollution 141, 115– 125. McGrath, S.P., Shen, Z.G., Zhao, F.J., 1997. Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant and Soil 188, 153–159. McGrath, S.P., Zhao, F.J., Lombi, E., 2001. Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant and Soil 232, 207–214. Novozamsky, I., Van Eck, R., Houba, V.J.G., Van der Lee, J.J., 1996. Solubilization of plant tissue with nitric acid-hydrofluoric acid-hydrogen peroxide in a closed system microwave digestor. Communications in Soil Science and Plant Analysis 27, 867–875.
914
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L.D., Lasat, M.M., Garvin, D.F., Eide, D., Kochian, L.V., 2000. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proceedings of the National Academy of Sciences of the United States of America 97, 4956–4960. Rietra, R.P.J.J., Ro¨mkens, P.F.A.M., Japenga, J., 2004. Cadmium and Zinc in Soil and Arable Crops in the Kempen Region. Report No. 974. Alterra, Wageningen, The Netherlands (in Dutch). Robinson, B.H., Leblanc, M., Petit, D., Brooks, R.R., Kirkman, J.H., Gregg, P.E.H., 1998. The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant and Soil 203, 47–56. Ro¨mkens, P.F.A.M., Zeilmaker, M.J., Rietra, R.P.J.J., Kan, C.A., Van Eijkeren, J.C.H., Van Raamsdonk, L.W.D., Lijzen, J.P.A., 2007. Exposure to and Uptake of Cadmium by Bovine Animals in the Kempen Region: a Model Study. Report No. 1438. Alterra, Wageningen, The Netherlands (in Dutch). Sauve´, S., Hendershot, W., Allen, H.E., 2000. Solid–solution partitioning of metals in contaminated soils: dependence on pH, total metal burden, and organic matter. Environmental Science & Technology 34, 1125–1131. Schwartz, C., Echevarria, G., Morel, J.L., 2003. Phytoextraction of cadmium with Thlaspi caerulescens. Plant and Soil 249, 27–35. Tipping, E., Rieuwerts, J., Pan, G., Ashmore, M.R., Lofts, S., Hill, M.T.R., Farago, M.E., Thornton, I., 2003. The solid–solution partitioning of heavy metals (Cu, Zn, Cd, Pb) in upland soils of England and Wales. Environmental Pollution 125, 213–225.
Van Nevel, L., Mertens, J., Oorts, K., Verheyen, K., 2007. Phytoextraction of metals from soils: how far from practice? Environmental Pollution 150, 34–40. Vellinga, T.V., Andre´, G., 1999. Sixty years of Dutch nitrogen fertiliser experiments, an overview of the effects of soil type, fertiliser input, management and of developments in time. Netherlands Journal of Agricultural Science 47, 215–241. Weng, L., Temminghoff, E.J.M., Van Riemsdijk, W.H., 2001. Contribution of individual sorbents to the control of heavy metal activity in sandy soil. Environmental Science & Technology 35, 4436–4443. Whiting, S.N., Leake, J.R., McGrath, S.P., Baker, A.J.M., 2001. Assessment of Zn mobilization in the rhizosphere of Thlaspi caerulescens by bioassay with nonaccumulator plants and soil extraction. Plant and Soil 237, 147–156. Zhao, F.J., Hamon, R.E., Lombi, E., McLaughlin, M.J., McGrath, S.P., 2002. Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. Journal of Experimental Botany 53, 535–543. Zhao, F.J., Hamon, R.E., McLaughlin, M.J., 2001. Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytologist 151, 613–620. Zhao, F.J., Lombi, E., McGrath, S.P., 2003. Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant and Soil 249, 37–43.
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Environmental Pollution journal homepage: www.elsevier.com/locate/envpol
Feasibility of phytoextraction to remediate cadmium and zinc contaminated soils G.F. Koopmans a, *, P.F.A.M. Ro¨mkens b, M.J. Fokkema b, J. Song c, Y.M. Luo c, J. Japenga b, F.J. Zhao d a
Department of Soil Quality, Wageningen University, Wageningen University and Research Centre (WUR), P.O. Box 47, 6700 AA, Wageningen, The Netherlands Alterra, WUR, P.O. Box 47, 6700 AA, Wageningen, The Netherlands c Soil and Environmental Bioremediation Research Centre, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, PR China d Soil Science Department, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK b
An experimental method is presented to be used to estimate the phytoextraction duration of a metal contaminated soil.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 February 2008 Received in revised form 8 May 2008 Accepted 12 May 2008
A Cd and Zn contaminated soil was mixed and equilibrated with an uncontaminated, but otherwise similar soil to establish a gradient in soil contamination levels. Growth of Thlaspi caerulescens (Ganges ecotype) significantly decreased the metal concentrations in soil solution. Plant uptake of Cd and Zn exceeded the decrease of the soluble metal concentrations by several orders of magnitude. Hence, desorption of metals must have occurred to maintain the soil solution concentrations. A coupled regression model was developed to describe the transfer of metals from soil to solution and plant shoots. This model was applied to estimate the phytoextraction duration required to decrease the soil Cd concentration from 10 to 0.5 mg kg1. A biomass production of 1 and 5 t dm ha1 yr1 yields a duration of 42 and 11 yr, respectively. Successful phytoextraction operations based on T. caerulescens require an increased biomass production. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Phytoextraction Cadmium Zinc Hyperaccumulator Thlaspi caerulescens Soil remediation
1. Introduction Contamination of soils with Cd and Zn is a ubiquitous problem all over the world. For example, soils in the Kempen region located in the south of The Netherlands are enriched with Cd and Zn, due to atmospheric emission of metal-bearing dust from a Zn ore smelter near the village of Budel (Fig. 1). This has resulted in a wide-spread diffuse contamination of soil affecting an area of about 350 km2 (Copius Peereboom-Stegeman and Copius Peereboom, 1989). Total Cd concentration in soil ranges from 5 to 10 mg kg1 in the immediate vicinity of this Zn ore smelter to less than 0.5 mg kg1 (background level) at a distance of 30 km. Although a total Cd concentration between 1 and 5 mg kg1 is not considered to be highly toxic, it still can cause environmental problems. Soils in the Kempen region are mostly sandy and acidic (pH < 5.5) with a low Soil Organic Matter (SOM) content (<4%). This combination of soil properties leads to a high availability of Cd and Zn in soil solution resulting in increased leaching (Degryse and Smolders, 2006) and uptake by arable crops and vegetables (Copius Peereboom-Stegeman and Copius Peereboom, 1989; Boekhold and Van der Zee,
* Corresponding author. Tel.: þ31 317 483842; fax: þ31 317 419000. E-mail address: [email protected] (G.F. Koopmans). 0269-7491/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2008.05.029
1994). Moreover, Cd and Zn levels in grass and maize from the Kempen region have been demonstrated to exceed the limit set by the European Union (EU) for animal fodder (Directive 2005/87/EC) (Rietra et al., 2004). This can, in turn, lead to increased metal levels in kidneys and liver of grazing animals beyond food quality standards of the EU (Directive 2001/466/EC) (Ro¨mkens et al., 2007). To improve conditions for grazing animals and to ultimately prevent effects on human health through food-chain accumulation, measures have to be taken to reduce transfer of Cd and Zn from soil to animal fodder. Due to the extensive size of the contaminated area in the Kempen region, use of conventional soil remediation techniques to remove metals from soil is not a feasible option. Alternatively, phytoextraction has to be considered as a measure to remediate metal contaminated soils in this region. Phytoextraction has gained world-wide attention as an environmentally friendly and potentially cost-effective technique to remove metals from soil. The use of hyperaccumulating plant species has been suggested as a promising strategy for phytoextraction (McGrath et al., 2001). Hyperaccumulators are defined as higher plants capable of accumulating >100 mg Cd kg1, >1000 mg Cu, Ni, and Pb kg1, and >10,000 mg Zn kg1 in the dry matter (dm) of shoots when growing in their natural habitats (Baker and Brooks, 1989). Many authors have proposed the use of the hyperaccumulator Thlaspi caerulescens J. & C. Presl to remediate
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pools in soil needs to be determined. Recently, a simple experimental method has been developed to achieve this goal (Japenga et al., 2007; Koopmans et al., 2007). This method involves a pot experiment in which a contaminated soil is mixed and equilibrated with an uncontaminated, but otherwise similar soil to establish a gradient in soil contamination levels reflecting the decrease, which would have been realized by phytoextraction. After one cropping cycle with the plant species of interest, regression-based log–log relationships are obtained describing the transfer of metals between the soil solid phase and soil solution as well as the accumulation of metals in plant shoots from soil solution. The coefficients of these regression models are highly soil- and plantspecific and can be implemented in a dynamic mass balance model to simulate the decrease in metal uptake with time resulting from the decrease of the sorbed metal pools in soil and to obtain a more realistic estimate of the phytoextraction duration. However, the experimental method of Japenga et al. (2007) and Koopmans et al. (2007) was only tested on a fictive soil created by spiking an uncontaminated soil with a heavily contaminated soil. The objective of our study was to test the potential of this method to predict the phytoextraction duration for a real case of soil metal contamination. For this purpose, a Cd and Zn contaminated soil from the Kempen region was used as a case study. We used the Ganges ecotype of T. caerulescens for remediation, because it can hyperaccumulate Zn just as other ecotypes, but it is far superior with respect to Cd accumulation (Lombi et al., 2000; Hutchinson et al., 2000; Assunça˜o et al., 2003a). Also, Lolium perenne L. was used, because grassland production for dairy farming is the main agricultural land use in the Kempen region. The outcome of this study can be used to facilitate the decision on whether phytoextraction is a feasible option to remediate metal contaminated soils in this region. 2. Material and methods 2.1. Soils Fig. 1. Location of the Kempen region. Contaminated soil was sampled from a nature reserve near Neerpelt in Belgium, whereas uncontaminated soil was sampled from a dairy farm near Soerendonk in The Netherlands. In the Dutch part of the Kempen region, an area of about 350 km2 is contaminated with Cd and Zn, due to emission of metal-bearing dust from a Zn ore smelter near Budel.
contaminated soils with moderate total but high available Cd and Zn concentrations (Baker et al., 1994; Brown et al., 1994; Knight et al., 1997; McGrath et al., 1997, 2006; Robinson et al., 1998; Hammer and Keller, 2003; Schwartz et al., 2003; Zhao et al., 2003; Maxted et al., 2007). However, the uncertainty of the time required to realize the desired target level in soil is one of the major constraints hampering the application of phytoextraction in practice. Long-term field experiments are not available, and estimates of the phytoextraction duration have to be based on model calculations (Maxted et al., 2007; Van Nevel et al., 2007). Removal rates of metals by plants from contaminated soils are highly dependent on soil properties, degree and bioavailability of metal contamination, and, obviously, metal uptake characteristics and biomass production of the plant species used for remediation (Lasat, 2000). Also, bioavailable metal pools in soil decrease during phytoextraction (Hammer and Keller, 2002; Keller and Hammer, 2004), which leads to a decrease of metal uptake by plants and lower metal removal rates. For example, Cd concentration in shoots of T. caerulescens decreased by a factor of 1.4 after three successive croppings on a metal contaminated soil (Keller and Hammer, 2004). Therefore, model calculations based on constant metal uptake can lead to underestimation of the phytoextraction duration. To obtain a more realistic estimate of the time required to clean up a specific contaminated soil, the response of the plant species of interest to the decrease of bioavailable metal
Soils were sampled from two sites near the Dutch–Belgian border in the Kempen region (Fig. 1). An acidic sandy soil collected from the 0 to 10 cm layer of a nature reserve near Neerpelt in Belgium was used as a source of contaminated soil. This area has been contaminated with Cd and Zn, due to atmospheric deposition of metal-bearing dust from a Belgian Zn ore smelter. The site was covered by a dense grass vegetation. An uncontaminated acidic sandy soil was collected from the 0 to 25 cm layer of a dairy farm near Soerendonk in The Netherlands. The uncontaminated site was not cultivated at the time of sampling. Distance between the two sites is about 15 km, and both soils have developed from the same parent material under similar climatological conditions. After sampling, soils were airdried, sieved through a 10-mm sieve, and stored until further use. 2.2. Pot experiments A gradient of soil metal contamination was established by mixing air-dry contaminated soil with air-dry uncontaminated soil in a ratio of 100:0, 75:25, 50:50, 25:75, and 0:100% (based on weight). After mixing, subsamples were taken from the five bulk soils for chemical analysis and for determination of the water holding capacity (WHC). The maximal WHC of these soils was on average 309 2 mL kg1 (standard deviation). Bulk soils were watered with demineralized water up to 50% of the maximal WHC, and incubated for 3 months in plastic bags at 4 C in the dark. After incubation, soils were watered with demineralized water up to 60% of the maximal WHC, which roughly equals the moisture content of these soils at field capacity, and fertilized with 30 mg N (as NH4NO3), 15 mg P (as KH2PO4), and 10 mg S (as K2SO4) kg1 soil (based on air-dry weight). Since growth rates of L. perenne and T. caerulescens (Ganges ecotype) are different, pot experiments with both plant species had separate controls consisting of uncultivated pots. For each metal contamination level, two pots were filled for L. perenne, two pots for T. caerulescens, and two pots for the control resulting in a total of 30 pots. Cone-shaped plastic pots 18 cm in height with a top diameter of 18 cm and a bottom diameter of 14 cm were used. A plastic bag with seven small needle holes at the bottom to prevent anaerobic conditions in the potted soil was placed in each pot to prevent roots from growing out of the pot. Each pot was filled with 4 kg of soil (based on air-dry weight). To prevent salt damage to germinating plant seeds, the upper 1 cm soil layer did not receive fertilizer. A PVC tube with a diameter of 3 cm and a length of 17 cm was placed vertically in the middle of each pot with the lower 3 cm part of the tube below the soil
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914 surface. This lower 3 cm part has small holes allowing for watering of the soil. Each pot was placed on an individual saucer. About 6 g seeds of L. perenne or 60 seeds of T. caerulescens were sown on the soil surface of the pots. To obtain a uniform soil cover of the latter, an additional 60 seeds were sown on bare spots after 15 d. Pot experiments were performed in a greenhouse: temperature was maintained at 18 C at night and at 20 C during the day, relative humidity varied between 30 and 60%, and a 16 h day was provided through the use of artificial light to supplement natural light at an intensity of 400 W m2. Pots were watered daily up to 60% of the maximal WHC with demineralized water and rotated to equalize exposure to light. Some leaves of T. caerulescens turned purplish with time, possibly due to P deficiency. Therefore, 8 mg P (as KH2PO4) kg1 soil (based on air-dry weight) was applied after 57 and 88 d to each pot of the experiment with T. caerulescens. After about 63 d, Thrips tabaci infested on T. caerulescens growing on one of the duplicate pots containing 100% uncontaminated soil, and an insecticide had to be used for pest control. Pot experiments were harvested after 36 d for L. perenne and after 113 d for T. caerulescens. Shoots were cut just above the soil surface. Roots of L. perenne were collected by shaking off soil. For harvesting roots of T. caerulescens, soil was air-dried, and roots were collected after sieving the soil through a 2-mm sieve. Root samples from both plant species were thoroughly washed with tap water followed by washing with demineralized water. Dry weight of the plant samples was determined after drying at 70 C for 48 h. Soil samples were dried at 40 C for 48 h and sieved through a 2-mm sieve.
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solution and sorbed metal pools. Transformation of metals in the sorbed form to more occluded forms was assumed to be negligible (De Vries et al., 2002). Leaching loss was calculated as the metal concentration in soil solution multiplied by the downward water flux from the 0 to 20 cm soil layer. We used 300 mm yr1 for the downward water flux, which is similar to the mean annual precipitation surplus in The Netherlands. Atmospheric deposition was set at 0.2 g Cd and 27.7 g Zn ha1 yr1 (Delahaye et al., 2003). The dynamic mass balance model was applied to estimate the phytoextraction duration of the 100% contaminated soil. Metal contamination was assumed to occur only in the 0–20 cm soil layer, which is similar to the shallow active rooting zone of T. caerulescens (Keller et al., 2003). We used 1.4 kg L1 for soil density. Biomass production of plants in pot experiments is often much higher than the production under field conditions (Delorme et al., 2000). Therefore, we used field data for the biomass production of L. perenne and T. caerulescens. Biomass production of permanent grassland in dairy farming on sandy soils in The Netherlands varies between 8 and 14 t dm ha1 yr1 (Vellinga and Andre´, 1999). In our model calculations, biomass production of L. perenne was set at these two outer values. Biomass production of T. caerulescens was set at 1 t dm ha1 yr1 (Robinson et al., 1998; Hammer and Keller, 2003; Keller et al., 2003; McGrath et al., 2006), whereas a value of 5 t dm ha1 yr1 was used to show the effect of an increased production on the phytoextraction duration.
3. Results and discussion
2.3. Chemical analyses
3.1. Soil properties Soil organic matter, reactive Al and Fe oxides, clay (<2 mm), unbuffered Cation Exchange Capacity (CEC), and total extractable metal concentrations of the five soils used for the pot experiments were determined using standard analytical procedures (Houba et al., 1997): SOM was determined by loss-on-ignition at 550 C, clay by the sieve and pipette method, reactive metal oxides by extraction with a mixture of ammonium oxalate and oxalic acid, CEC by the unbuffered 0.01 M BaCl2 method, and total extractable metal concentrations by digestion with aqua regia. Metal concentrations were measured with an Inductively Coupled Plasma-Atomic Emission Spectrometer (ICP-AES). Metals extractable with 0.43 M HNO3 (Houba et al., 1997) and pH and concentrations of Dissolved Organic Carbon (DOC) and metals in 1:10 (w/v) 0.01 M CaCl2 extracts (Houba et al., 2000) were determined before and after the pot experiments. The pH was measured with a combined glass-electrode, DOC with a fully automated segmented flow analyser (Skalar, SK12) by persulphate and tetraborate oxidation under ultraviolet light and infrared detection, and metal concentrations in the 0.43 M HNO3 and 0.01 M CaCl2 extracts with an ICP-AES and ICP-Mass Spectrometer (ICP-MS), respectively. Except for clay, all soil analyses were performed in duplicate. Dried plant shoots and roots were ground in a titanium grinder. Plant material was digested by microwave destruction (Novozamsky et al., 1996). Metal concentrations in the digests were measured with an ICP-MS. Quality of the analyses was monitored by including blanks and soil and plant standards in each batch and an interlaboratory exchange program. 2.4. Statistics Linear regression analyses were performed to derive models describing the transfer of metals between the soil solid phase and soil solution as well as the accumulation of metals in plant shoots from soil solution. For the sorbed metal pools in soil, results of the 0.43 M HNO3 extraction method were used. Metals extracted with HNO3 are considered as estimates of sorbed metals reacting with binding sites located on the surfaces of SOM, reactive metal oxides, and clay, and they control the metal concentrations in soil solution, whereas metals extracted with aqua regia include the more occluded forms (Weng et al., 2001; Tipping et al., 2003). Metal concentrations in the 0.01 M CaCl2 extracts were used as an estimate for metals in soil solution (Degryse et al., 2003). Metal concentrations in the soil solution extracts were determined before and after the pot experiments, whereas plant shoot metal concentrations were determined only at the end. Metal accumulation in plant shoots, however, is a reflection of the metal concentrations in soil solution occurring throughout the entire growth period. Therefore, plant shoot metal concentrations were compared to the mean of the metal concentrations in the soil solution extracts before and after the pot experiments. Duplicate pots were treated as individual samples. All data were log-transformed. Significance of R2adj and predictor variables was assessed using F-tests and t-tests, respectively. Least significant difference method with a 0.05 probability value was used to determine effects of (i) soil contamination level on shoot and root biomass and (ii) treatment (control versus planted pots) on sorbed metal pools and on pH and concentrations of DOC and metals in the soil solution extracts. Statistical analyses were performed with Genstat, Release 9.2. 2.5. Phytoextraction duration The regression models were implemented in a dynamic mass balance model similar to the approach used by De Vries et al. (2002). Changes in the sorbed metal pools in soil with time were predicted by adding input through atmospheric deposition and by subtracting outputs through leaching and plant uptake. During phytoextraction, equilibrium was assumed between metal concentrations in soil
Properties of the 100% uncontaminated soil used to dilute the 100% contaminated soil need to be as similar as possible to those of the latter so as to avoid changes in the solubility of metals after mixing (Japenga et al., 2007; Koopmans et al., 2007). In Table 1, selected properties of the five soils used for the pot experiments are presented. Differences in pH, SOM, the sum of reactive Al and Fe oxides ([Al þ Fe]ox), clay, CEC, and DOC between the 100% contaminated soil and the 100% uncontaminated soil were small in comparison with the high variability normally found for these soil properties in acidic sandy soils (Koopmans et al., 2006). Mixing caused pH to decrease gradually from 5.4 in the 100% contaminated soil to 5.1 in the 100% uncontaminated soil, SOM from 3.8 to 3.2%, [Al þ Fe]ox from 84.0 to 56.4 mmol kg1, and CEC from 52.3 to 41.3 mmol kg1, whereas DOC increased from 5.5 to 9.4 mg L1. Total metal concentrations in the 100% contaminated soil were 19 (Cd) and 13 (Zn) times greater than the Dutch target values of 0.5 mg Cd and 60 mg Zn kg1 soil. In the 100% uncontaminated soil, the total Zn concentration was lower than the Dutch target value, whereas total Cd was the same as the target value. Sorbed metal pools accounted for on average 94% (Cd) and 78% (Zn) of the total metal concentrations. Hence, most of the total metal concentrations can exchange with soil solution and can become available with time for plant uptake. 3.2. Plant growth and metal concentrations Shoot biomass of L. perenne was constant for most soils, but decreased significantly for the 100% contaminated soil (Table 2). This may be due to metal phytotoxicity, because L. perenne grown on this soil had clearly visible chlorosis symptoms. In contrast, shoot biomass of T. caerulescens grown on the 100% uncontaminated soil decreased significantly compared to the other soils (Table 2). This may, in part, be explained by infestation with T. tabaci of T. caerulescens grown on one of the duplicate pots containing this soil leading to a premature senescence of leaves. T. caerulescens grown on this pot was possibly more susceptible to thrips, because shoots of these plants contained much less Cd than those of the plants grown on the other soils (Table 2). Hyperaccumulation of Cd can protect T. caerulescens from leaf feeding damage by thrips (Jiang et al., 2005). Metal concentrations in shoots of T. caerulescens were between 165 and 279 (Cd) and between 5 and 51 (Zn) times higher than those in shoots of L. perenne (Table 2), emphasizing the great ability of T. caerulescens to take up and translocate these metals from roots
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Table 1 Soil properties of the contaminated soil and uncontaminated soil and intermediate soil mixtures before the start of the pot experiments Contaminated soil (%)
100 75 50 25 0
pHa
SOMb (%)
5.4 0.03 5.3 0.01 5.3 0.01 5.2 0.00 5.1 0.01
3.8 0.0 3.7 0.2 3.5 0.1 3.3 0.1 3.2 0.1
[Al þ Fe]oxc (mmol kg1)
Clay (%)
84.0 1.2 79.5 0.4 72.7 1.2 66.1 0.6 56.4 1.0
2 3 2 2 2
CECd (mmol kg1)
52.3 0.5 54.6 0.6 53.3 1.6 47.4 0.6 41.3 1.3
DOCa (mg L1)
5.5 0.2 6.7 0.1 8.1 0.7 9.3 0.6 9.4 0.1
Dissolved metal concentrationa
Sorbed metal concentratione
Total metal concentrationf
Cd (mg L1)
Zn (mg L1)
Cd (mg kg1)
Zn (mg kg1)
Cd (mg kg1)
Zn (mg kg1)
201 6 162 2 120 1 62.6 0.2 8.4 0.5
13.7 0.4 10.6 0.2 7.7 0.0 4.0 0.0 0.32 0.03
10.2 0.4 7.9 0.4 5.0 0.3 2.7 0.2 0.45 0.02
689 26 516 25 379 28 181 18 16.1 0.8
9.8 0.6 8.5 0.4 5.6 0.0 3.0 0.1 0.51 0.03
776 43 660 29 423 4 212 2 33.3 1.4
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
Values represent mean standard deviation of the duplicate analyses. a Measured in 0.01 M CaCl2 extracts. b Soil Organic Matter (SOM). c Reactive Al and Fe oxides extracted with a mixture of ammonium oxalate and oxalic acid ([Al þ Fe]ox). d Unbuffered Cation Exchange Capacity (CEC). e Sorbed metal concentrations extracted with 0.43 M HNO3. f Total extractable soil metal concentrations determined by digestion with aqua regia.
Table 2 Biomasss production of shoot and roots, shoot and root Cd and Zn concentrations, and Cd and Zn shoot:root ratios of L. perenne and T. caerulescens Contaminated soil (%)
100 75 50 25 0
L. perenne
T. caerulescens
Shoots (g pot1)
Roots (g pot1)
11.2 0.1a 13.7 0.6b 13.7 0.4b 14.2 0.4b 13.5 0.3b
6.7 0.3a 7.1 0.1a 7.2 0.7a 10.4 3.3a 8.9 1.1a
Shoots
Roots
Shoot:root ratio
Cd (mg kg1)
Zn (mg kg1)
Cd (mg kg1)
Zn (mg kg1)
Cd
Zn
3.5 0.1 2.7 0.2 2.0 0.1 1.2 0.1 0.27 0.03
824 9 621 7 470 6 245 2 40.7 2.6
47.9 0.1 33.3 1.0 22.7 1.2 15.3 0.4 3.7 0.3
3734 28 2342 56 1638 2 944 23 175 4
0.07 0.00 0.08 0.01 0.09 0.01 0.08 0.01 0.07 0.00
0.22 0.00 0.27 0.01 0.29 0.00 0.26 0.00 0.23 0.01
Shoots (g pot1)
Roots (g pot1)
15.6 0.0a 15.6 0.1a 15.5 2.0a 15.7 0.6a 10.8 2.0b
4.3 0.0ab 4.6 0.2a 5.3 0.3a 4.1 0.5ab 3.1 1.2b
Shoots
Roots
Shoot:root ratio
Cd (mg kg1)
Zn (mg kg1)
Cd (mg kg1)
Zn (mg kg1)
Cd
Zn
749 73 694 0 561 81 270 23 43.9 7.8
4044 400 4321 357 4264 341 3776 60 2081 105
375 1 349 12 269 13 272 54 92.4 0.7
1441 21 1228 15 1177 43 895 85 389 123
2.0 0.2 2.0 0.1 2.1 0.2 1.0 0.1 0.48 0.09
2.8 0.2 3.5 0.3 3.6 0.4 4.2 0.5 5.6 1.5
Means of biomasss production of shoot and roots for L. perenne and T. caerulescens within 1 column followed by different letters are significantly different at the P < 0.05 level. Values represent mean standard deviation of the duplicate pots.
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
to shoots. Metal concentrations in shoots of L. perenne were much smaller than those in roots. Consequently, shoot:root ratios of Cd and Zn were far below 1 for this plant species (Table 2), which is typical for nonhyperaccumulating plants (McGrath et al., 2001). In contrast to L. perenne, metal concentrations in shoots of T. caerulescens were much greater than those in roots. The shoot:root ratio of Cd was above 1 for most soils (Table 2). Hyperaccumulating plant species usually have a shoot:root ratio above 1 (McGrath et al., 2001). For most soils, the Cd concentration in shoots of T. caerulescens by far exceeded the hyperaccumulation level of 100 mg kg1 (Table 2), as defined by Baker and Brooks (1989). This Cd hyperaccumulation trait is typical for the Ganges ecotype (Lombi et al., 2000; Hutchinson et al., 2000). The shoot:root ratio of Zn was above 1 for all soils, although the Zn concentration in shoots
A
12
L. perenne Control
909
of T. caerulescens did not reach the hyperaccumulation level of 10,000 mg kg1 dm (Table 2) (Baker and Brooks, 1989). 3.3. Metal pools Growth of L. perenne hardly changed the sorbed metal pools, whereas the sorbed Cd pool decreased significantly for most soils after one cropping of T. caerulescens (Fig. 2). The extent of this reduction varied between 43 and 57% emphasizing the great ability of the Ganges ecotype to remove Cd from soil. Three successive croppings of a Cd hyperaccumulating ecotype of T. caerulescens on a metal contaminated acidic soil resulted in a similar reduction of 59% of the 2 M HNO3-extractable Cd pool in a pot experiment of Keller and Hammer (2004). The sorbed Zn pool decreased by 7–52%
B
12
T. caerulescens
a
Control
a a 10
a
a a
8
6
Sorbed Cd (mg kg-1)
Sorbed Cd (mg kg-1)
10
a a
4
8 b 6
a b
4
a a b 2
a
2
b
a a 0
100
75
50
25
a a 0
0
100
C
800
L. perenne
D
50
800
25
0
T. caerulescens
a
Control
a b
75
Contaminated soil (%)
Contaminated soil (%)
Control
b
600
600 a a
Sorbed Zn (mg kg-1)
Sorbed Zn (mg kg-1)
a b
a a
400
a a
200
400
a a
a a
200
a a
a a 0
100
75
50
25
Contaminated soil (%)
0
0
100
75
50
25
0
Contaminated soil (%)
Fig. 2. Sorbed Cd (A and B) and Zn pools (C and D) in the soil samples taken after the pot experiments with L. perenne (A and C) and T. caerulescens (B and D). Values of the control represent mean standard deviation of the duplicate analyses, whereas values of the planted pots represent mean standard deviation of the duplicate pots. Means with different letters are significantly different at the P < 0.05 level.
12.5 0.9b 10.6 0.1b 6.9 0.0b 3.2 0.0a 0.11 0.03a Values of the control pots represent mean standard deviation of the duplicate analyses, whereas values for the planted pots represent mean standard deviation of the duplicate pots. Means of pH, DOC, and total dissolved Cd and Zn concentrations for L. perenne and T. caerulescens within one row followed by different letters are significantly different at the P < 0.05 level.
14.1 0.6a 12.1 0.0a 9.1 0.6a 4.4 0.1a 0.40 0.00a
Control Plant
98.7 1.2b 69.7 2.4b 41.1 1.7b 20.6 1.9b 2.8 0.5b 200 9a 169 1a 128 6a 66.0 0.8a 9.5 0.1a
Control Plant
7.8 0.1b 10.1 0.1b 9.9 0.2b 9.8 1.0b 9.9 0.4a 5.1 0.6a 7.5 0.0a 6.9 0.3a 6.9 0.0a 11.3 0.7a
Control Plant
5.4 0.01b 5.2 0.03a 5.1 0.00b 5.1 0.01b 5.0 0.00b 5.3 0.01a 5.2 0.03a 5.1 0.01a 5.0 0.00a 4.8 0.02a
Control Plant
14.4 0.3b 11.1 0.0a 8.1 0.2a 4.2 0.1a 0.34 0.00a 15.0 0.1a 11.4 0.3a 8.3 0.0a 4.4 0.1a 0.33 0.00a
Control Plant
211 1b 169 0a 122 3a 65.3 1.0a 8.8 0.1a 217 0a 174 4a 126 1a 66.7 0.8a 8.5 0.1a
Control Plant
4.7 0.1a 6.2 0.4a 7.2 0.0a 8.9 0.5a 9.2 0.0a 4.9 0.3a 6.5 0.0a 7.7 0.3a 9.1 0.2a 8.8 0.3a
Control
5.4 0.01a 5.3 0.01a 5.2 0.04a 5.1 0.00a 4.9 0.01a
Plant Control
5.3 0.04a 5.3 0.01a 5.2 0.00a 5.1 0.01a 5.0 0.00a 100 75 50 25 0
Zn (mg L1) Cd (mg L1) DOC (mg L1) pH
T. caerulescens
Zn (mg L1) Cd (mg L1) DOC (mg L1) pH
Metal concentrations in the soil solution extracts could be very well predicted from the sorbed metal pools with R2adj values of 98.7% (Cd) and 99.3% (Zn) (Fig. 3). Although pH and other soil properties (SOM and Alox) contributed significantly to the regression models of Cd and Zn, R2adj only slightly further improved by including these soil properties (not shown). Obviously, pH has to be included when comparing soils with a wide pH range (Sauve´ et al., 2000; Tipping et al., 2003). In our experimental set-up, however, differences in pH as well as in other soil properties were deliberately minimized so as to avoid changes in metal solubility after mixing the 100% contaminated soil with the 100% uncontaminated soil. The sum of the metal uptake in the shoots and roots of T. caerulescens was 2.8–3.3 (Cd) and 0.8–2.0 (Zn) times greater than the decrease of the metal concentrations in the soil solution extracts (not shown). Hence, replenishment of Cd and Zn in the soil solution extracts must have occurred through the release of metals bound to the soil solid phase. Replenishment of bioavailable metal pools during cropping of T. caerulescens on metal contaminated soils has been reported previously (Knight et al., 1997; Whiting et al., 2001; Hammer and Keller, 2002; Keller and Hammer, 2004). This gives rise to the question whether a new equilibrium has been established between metal concentrations in the soil solution extracts and metals bound to the soil solid phase after one cropping of
L. perenne
3.4. Regression models
Contaminated soil (%)
after one cropping of T. caerulescens, although this reduction was only significant for the 100% contaminated soil (Fig. 2). The sum of the Cd uptake in the shoots and roots of T. caerulescens accounted for 74 to 89% of the decrease of the sorbed Cd pool (not shown). However, the Cd concentration measured in roots may overestimate the amount of Cd actually taken up by roots, because Cd in roots of T. caerulescens not only includes Cd in the root symplast, but also Cd bound in the apoplast (Zhao et al., 2002). Growth of L. perenne hardly affected the composition of the soil solution extracts, whereas metal concentrations decreased significantly for most soils after one cropping of T. caerulescens (Table 3). The extent of this reduction varied between 51 and 71% for Cd and between 12 and 72% for Zn. Hence, T. caerulescens seems to have potential to reduce the readily bioavailable metal pools in soil, a concept referred to as Bioavailable Contaminant Stripping (BCS) (Hamon and McLaughlin, 1999). The purpose of BCS is to reduce environmental risks posed by the presence of metals in soil through decreasing the readily bioavailable metal pools within a limited number of croppings instead of decreasing the total metal concentrations. For an environmentally safe application, kinetics of metal replenishment in soil solution after BCS has been applied need to be understood. Release of metals from the soil solid phase can increase the environmental risks again in case of a disequilibrium between metal concentrations in soil solution and metals bound to the soil solid phase. This issue will be discussed in more detail in the next paragraph. Growth of T. caerulescens resulted in small, but significant increases in pH and DOC for most soils (Table 3). Apparently, the ability of this plant species to remove metals from our soils was not related to rhizosphere acidification, which is in agreement with previous studies (Knight et al., 1997; McGrath et al., 1997; Hutchinson et al., 2000; Schwartz et al., 2003). Increase of DOC may be due to the release of root exudates by T. caerulescens, but this mechanism is known not to be involved in the metal hyperaccumulation behavior of the Ganges ecotype (Zhao et al., 2001). Hyperaccumulation of metals by T. caerulescens is likely to involve multiple traits, with enhanced metal uptake, root to shoot translocation, and vacuolar sequestration in leaf cells at least being partly under genetic control (Assunça˜o et al., 2003b).
Plant
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
Table 3 The pH and DOC and Cd and Zn concentrations in the 0.01 M CaCl2 extracts obtained from the soil samples of the pot experiments with L. perenne and T. caerulescens
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A
B
2.5
4.5
4.0
1.5 Initial soils Control L. perenne Control T. caerulescens
1.0
log y = 1.29 ± 0.01*** + (1.06 ± 0.02*** log x)
0.5
R
0.0 -1.0
-0.5
0.0
2 adj
Log dissolved Zn (µg L-1)
2.0
Log dissolved Cd (µg L-1)
911
= 98.7%*** (n = 35)
0.5
1.0
Log sorbed Cd (mg
3.5
Initial soils Control L. perenne Control T. caerulescens
3.0
2.5
log y = 1.29 ± 0.03*** + (1.02 ± 0.01*** log x) 2 R adj = 99.3%*** (n = 35)
2.0
1.5 0.5
1.5
kg-1)
1.0
1.5
2.0
2.5
3.0
Log sorbed Zn (mg kg-1)
Fig. 3. Cadmium (A) and Zn concentrations (B) in the 1:10 (w/v) 0.01 M CaCl2 extracts plotted against the sorbed metal pools with the regression model describing the soil solid phase–soil solution relationship (regression coefficients standard error). For the regression analysis, all soil samples were used including those taken before and after the pot experiments with L. perenne and T. caerulescens. Statistical significance: ***for P < 0.001.
T. caerulescens. Metal concentrations in the soil solution extracts seemed to be close to equilibrium with the sorbed metal pools, because partitioning of Cd and Zn between the solid phase of the bulk soil and soil solution could be described with a single regression model for all soil samples including those taken before and after the pot experiments with L. perenne and T. caerulescens (Fig. 3). Apparently, plant uptake of Cd and Zn was followed by instantaneous release of these metals from the soil solid phase and was not kinetically limited by desorption of these metals. This finding supports our assumption of equilibrium between metal concentrations in soil solution and sorbed metal pools as used in the dynamic mass balance model calculations to predict the phytoextraction duration. However, a local disequilibrium in the rhizosphere resulting from the sink effect induced by roots of T. caerulescens would not have been detected, because we mixed our soil samples before chemical analysis. Our hypothesis of an apparent equilibrium is supported by measurement of Cd and Zn desorption kinetics in soils with the technique of diffusive gradients in thin-
A
3.5
films (Ernstberger et al., 2005). In these experiments, desorption of Cd and Zn from the soil solid phase was not kinetically limited. Analogous to our finding, the inorganic P concentration in 0.01 M CaCl2 extracts of soil samples taken at various stages of a long-term pot experiment in which a highly P-enriched soil was remediated by 31 successive croppings of L. perenne was continuously in equilibrium with the sorbed P pool (Koopmans et al., 2004). The question whether equilibrium has indeed been reached in our pot experiments requires more investigation, but this falls outside the scope of this study. Hence, application of BCS to contaminated soils in the Kempen region may result in a stable decrease of the metal concentrations in soil solution with time. However, lack of legislative support hampers the application of BCS in practice, because legislation on soil remediation is still based on target values using total soil metal concentrations instead of chemically available pools (Keller and Hammer, 2004). Metal accumulation in plant shoots could be very well predicted from the metal concentrations in the soil solution extracts
B
4.0
3.0
2.0 1.5
log y = 0.98 ± 0.06*** + (0.89 ± 0.04*** log x) 2
R
adj
= 98.6%*** (n = 10)
1.0 L. perenne T. caerulescens
0.5 0.0
Log Zn shoots (mg kg-1)
Log Cd shoots (mg kg-1)
3.5 2.5
log y = 2.91 ± 0.07*** + (0.18 ± 0.02*** log x) 2
R
3.0
-1.0 0.5
L. perenne T. caerulescens
2.0
log y = -0.41 ± 0.08** + (0.79 ± 0.02*** log x) R
log y = -1.33 ± 0.04*** + (0.80 ± 0.02*** log x) R2adj = 99.3%*** (n = 10)
1.0
1.5
2.0
2.5
Log dissolved Cd (µg L-1)
91.3%*** (n = 10)
2.5
1.5 -0.5
adj=
1.0 2.0
2.5
3.0
2 adj
3.5
= 99.3%*** (n = 10)
4.0
4.5
Log dissolved Zn (µg L-1)
Fig. 4. Cadmium (A) and Zn concentrations (B) in the shoots of L. perenne and T. caerulescens plotted against metal concentrations in the 1:10 (w/v) 0.01 M CaCl2 extracts with the regression model describing the soil solution–plant relationship (regression coefficients standard error). Statistical significance: **for P < 0.01 and ***for P < 0.001.
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Table 4 Predicted phytoextraction duration to reach the Dutch target values (total metal concentrations of 0.5 mg Cd kg1 and 60 mg Zn kg1) in the 0–20 cm layer of the 100% contaminated soil from the Kempen region (Fig. 1) using L. perenne and T. caerulescens for remediation Metal
L. perenne 8 t ha (yr)
Cd Zn
128 91
1
yr
T. caerulescens 1
1
14 t ha (yr)
yr
1
124 82
1 t ha1 yr1 (yr)
5 t ha1 yr1 (yr)
42 82
11 45
Biomass production of L. perenne and T. caerulescens was set at 8 and 14 t ha1 yr1 and 1 and 5 t ha1 yr1, respectively.
with R2adj values of 99.3% (Cd and Zn) for L. perenne and 98.6% (Cd) and 91.3% (Zn) for T. caerulescens (Fig. 4). Accumulation of Cd in the shoots of L. perenne and T. caerulescens clearly increased with the dissolved Cd concentration. For Zn, L. perenne showed the same behavior, but the behavior of T. caerulescens was different. Accumulation of Zn in the shoots of T. caerulescens depended much less on the Zn concentration in the soil solution extracts. Enabled by a high-affinity Zn uptake mechanism in the roots, T. caerulescens is able to accumulate large amounts of Zn at a relatively constant rate from the solution phase over a wide range of Zn concentrations (Pence et al., 2000). This behavior is typical for Zn hyperaccumulating plant species, and the ability of different T. caerulescens ecotypes to hyperaccumulate Zn has been reported many times before (Hutchinson et al., 2000; Lombi et al., 2000; Assunça˜o et al., 2003a). 3.5. Phytoextraction duration The time required to realize the target value in the 0–20 cm layer of the 100% contaminated soil using a biomass production of 5 t dm ha1 yr1 for T. caerulescens was 11 yr for Cd, whereas 45 yr would be needed to clean up the Zn contamination (Table 4 and Fig. 5). Apparently, phytoextraction is more likely to be feasible for Cd than for Zn, which has been concluded previously (McGrath et al., 1997, 2006; Robinson et al., 1998; Hammer and Keller, 2003; Schwartz et al., 2003; Zhao et al., 2003). A biomass production of
A 11
5 t dm ha1 yr1 for T. caerulescens, however, is unrealistically high, because the production of this plant species in field experiments has been reported to vary around 1–2 t dm ha1 yr1 (Robinson et al., 1998; Hammer and Keller, 2003; Keller et al., 2003; McGrath et al., 2006). The phytoextraction duration for the 100% contaminated soil increased to 42 yr for Cd and to 82 yr for Zn using a biomass production of 1 t dm ha1 yr1 for T. caerulescens, whereas the phytoextraction duration using L. perenne for remediation was (much) longer (Table 4). Moreover, we estimated the phytoextraction duration for soils with a lower initial sorbed Cd concentration, which are located at further distance from the Zn ore smelter, using T. caerulescens for remediation and a biomass production of 1 t dm ha1 yr1. Phytoextraction duration decreased from 42 yr for a soil with 10.2 mg Cd kg1 to 10 yr for a soil with 1 mg Cd kg1 (Fig. 6). Since any phytoextraction duration exceeding 10 yr would be totally uneconomic (Robinson et al., 1998), phytoextraction does not seem to be a feasible option for the remediation of metal contaminated soils in the Kempen region at present. Hence, the technique of phytoextraction clearly needs to be improved before it is ready for application in practice (Van Nevel et al., 2007). The major constraint, which seems to reduce the phytoextraction effectiveness of T. caerulescens, is the low biomass production of this plant species under field conditions. The biomass production of T. caerulescens can be increased with improved knowledge of agricultural management practices and screening and plant breeding (Zhao et al., 2003). For example, N fertilizer application increased the biomass production of this plant species resulting in greater metal removal rates (Schwartz et al., 2003). Fertilizing crops of T. caerulescens grown in base-mine tailings increased biomass production by a factor of 2–3 without significant reductions of shoot metal concentrations (Bennett et al., 1998). A biomass production of 5 t dm ha1 yr1, therefore, may be achievable for T. caerulescens (Zhao et al., 2003). Using this biomass production, phytoextraction duration decreased from 11 yr for a soil with 10.2 mg Cd kg1 to 3 yr for a soil with 1 mg Cd kg1 (Fig. 6). Hence, phytoextraction using T. caerulescens holds promise to remediate contaminated soils with moderate total Cd concentrations in the future, but improvement of this technique by increasing the biomass production of this plant species is a prerequisite.
B
10
800 700 600
8
Sorbed Zn (mg kg-1)
Sorbed Cd (mg kg-1)
9
7 6 5 4 3
400 300 1 t dm ha-1 yr-1
200
2
1 t dm ha-1 yr-1
100
1 0
500
5 t dm ha-1 yr-1
0
10
20
30
40
Time (yr)
50
60
70
0
Target value
5 t dm ha-1 yr-1
Target value
0
20
40
60
80
100
120
Time (yr)
Fig. 5. Modelled decrease of the sorbed Cd (A) and Zn pools (B) in the 0–20 cm layer of the 100% contaminated soil from the Kempen region (Fig. 1) with time, predicted by calculating the metal concentrations in the shoots of T. caerulescens and leaching as a log-linear function of the metal concentrations in the soil solution extracts (Fig. 4). Partitioning of metals between soil solid phase and soil solution was calculated using the regression models presented in Fig. 3. A biomass production of 1 and 5 t dm ha1 yr1 was used in the model calculations. Number of harvests required to complete phytoextraction can be read from the x-axis of the figure as the number of years assuming one annual harvest.
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
50
40
-1
-1
Phytoextraction duration (yr)
1 t dm ha yr
30
20
-1
5 t dm ha yr
-1
10
0
1
2
3
4
5
6
7
8
9
10
11
Initial sorbed Cd pool (mg kg-1) Fig. 6. Time required to remediate the 0–20 cm layer of soils from the Kempen region (Fig. 1) as a function of the initial sorbed Cd pool in soil, predicted by calculating the metal concentrations in the shoots of T. caerulescens and leaching as a log-linear function of the metal concentrations in soil solution (Fig. 4). Partitioning of Cd between the soil solid phase and soil solution was calculated using the regression model presented in Fig. 3. A biomass production of 1 and 5 t dm ha1 yr1 was used in the model calculations.
Acknowledgements The authors kindly acknowledge Erik Smolders and Fien Degryse and the Beheersteam Hageven for help in selecting and locating the contaminated soil in the nature reserve het Hageven. This project was financed by the Chinese Ministry of Science and Technology (contract no. 2006DFA91940 and 2004CB720403) and the Royal Dutch Academy of Sciences (contract no. 04-PSA-E-05). Rothamsted Research receives grant-aided support from the UK Biotechnology and Biological Sciences Research Council.
References Assunça˜o, A.G.L., Bookum, W.M., Nelissen, H.J.M., Vooijs, R., Schat, H., Ernst, W.H.O., 2003a. Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytologist 159, 411–419. Assunça˜o, A.G.L., Schat, H., Aarts, M.G.M., 2003b. Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytologist 159, 351–360. Baker, A.J.M., Brooks, R.R., 1989. Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126. Baker, A.J.M., McGrath, S.P., Sidoli, C.M.D., Reeves, R.D., 1994. The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resources, Conservation and Recycling 11, 41–49. Bennett, F.A., Tyler, E.K., Brooks, R.R., Gregg, P.E.H., Stewart, R.B., 1998. Fertilisation of hyperaccumulators to enhance their potential for phytoremediation and phytomining. In: Brooks, R.R. (Ed.), Plants that Hyperaccumulate Heavy Metals. CAB International, Wallingford, UK, pp. 249–259. Boekhold, A.E., Van der Zee, S.E.A.T.M., 1994. Field scale variability of cadmium and zinc in soil and barley. Environmental Monitoring and Assessment 29, 1–15. Brown, S.L., Chaney, R.L., Angle, J.S., Baker, A.J.M., 1994. Phytoremediation potential of Thlaspi caerulescens and bladder campion for zinc- and cadmiumcontaminated soil. Journal of Environmental Quality 23, 1151–1157. Copius Peereboom-Stegeman, J.H.J., Copius Peereboom, J.W., 1989. The intake of cadmium in the Kempen, an area in the south of the Netherlands. Ecotoxicology and Environmental Safety 18, 93–108.
913
Degryse, F., Broos, K., Smolders, E., Merckx, R., 2003. Soil solution concentration of Cd and Zn can be predicted with a CaCl2 soil extract. European Journal of Soil Science 54, 149–157. Degryse, F., Smolders, E., 2006. Mobility of Cd and Zn in polluted and unpolluted Spodosols. European Journal of Soil Science 57, 122–133. Delahaye, R., Fong, P.K.N., Van Eerdt, M.M., Van der Hoek, K.W., Olsthoorn, C.S.M., 2003. Emission of Seven Heavy Metals to Agricultural Land. Centraal Bureau voor de Statistiek, Voorburg, The Netherlands (in Dutch). Delorme, T.A., Angle, J.S., Coale, F.J., Chaney, R.L., 2000. Phytoremediation of phosphorus-enriched soils. International Journal of Phytoremediation 2, 173–181. De Vries, W., Ro¨mkens, P.F.A.M., Van Leeuwen, T., Bronswijk, J.J.B., 2002. Heavy metals. In: Haygarth, P.M., Jarvis, S.C. (Eds.), Agriculture, Hydrology and Water Quality. CAB International, Wallingford, pp. 107–132. Ernstberger, H., Zhang, H., Tye, A., Young, S., Davison, W., 2005. Desorption kinetics of Cd, Zn, and Ni measured in soils by DGT. Environmental Science & Technology 39, 1591–1597. Hammer, D., Keller, C., 2002. Changes in the rhizosphere of metal-accumulating plants evidenced by chemical extractants. Journal of Environmental Quality 31, 1561–1569. Hammer, D., Keller, C., 2003. Phytoextraction of Cd and Zn with Thlaspi caerulescens in field trials. Soil Use and Management 19, 144–149. Hamon, R.E., McLaughlin, M.J., 1999. Use of the hyperaccumulator Thlaspi caerulescens for bioavailable contaminent stripping. In: Wenzel, W.W., Adriano, D.C., Alloway, B., Doner, H., Keller, C., Lepp, N.W., Mench, M., Naidu, R., Pierzynski, G. M. (Eds.), Proceedings of the Fifth International Conference on the Biogeochemistry of Trace Elements (ICOBTE), 12–15 July, 1999, Vienna, Austria, pp. 908–909. Houba, V.J.G., Temminghoff, E.J.M., Gaikhorst, G.A., Van Vark, W., 2000. Soil analysis procedures using 0.01 M calcium chloride as extraction reagent. Communications in Soil Science and Plant Analysis 31, 1299–1396. Houba, V.J.G., Van der Lee, J.J.G., Novozamsky, I., 1997. Soil and Plant Analysis. Part 1: Soil Analysis Procedures. Wageningen University, Wageningen, The Netherlands. Hutchinson, J.J., Young, S.D., McGrath, S.P., West, H.M., Black, C.R., Baker, A.J.M., 2000. Determining uptake of ‘non-labile’ soil cadmium by Thlaspi caerulescens using isotopic dilution techniques. New Phytologist 146, 453–460. Japenga, J., Koopmans, G.F., Song, J., Ro¨mkens, P.F.A.M., 2007. A feasibility test to estimate the duration of phytoextraction of heavy metals from polluted soils. International Journal of Phytoremediation 9, 115–132. Jiang, R.F., Ma, D.Y., Zhao, F.J., McGrath, S.P., 2005. Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytologist 167, 805–814. Keller, C., Hammer, D., 2004. Metal availability and soil toxicity after repeated croppings of Thlaspi caerulescens in metal contaminated soils. Environmental Pollution 131, 243–254. Keller, C., Hammer, D., Kayser, A., Richner, W., Brodbeck, M., Sennhauser, M., 2003. Root development and heavy metal phytoextraction efficiency: comparison of different plant species in the field. Plant and Soil 249, 67–81. Knight, B., Zhao, F.J., McGrath, S.P., Shen, Z.G., 1997. Zinc and cadmium uptake by the hyperaccumulator Thlaspi caerulescens in contaminated soils and its effects on the concentration and chemical speciation of metals in soil solution. Plant and Soil 197, 71–78. Koopmans, G.F., Chardon, W.J., Dekker, P.H.M., Ro¨mkens, P.F.A.M., Schoumans, O.F., 2006. Comparing different extraction methods for estimating phosphorus solubility in various soil types. Soil Science 171, 103–116. Koopmans, G.F., Chardon, W.J., Ehlert, P.A.I., Dolfing, J., Suurs, R.A.A., Oenema, O., Van Riemsdijk, W.H., 2004. Phosphorus availability for plant uptake in a phosphorus-enriched noncalcareous sandy soil. Journal of Environmental Quality 33, 965–975. Koopmans, G.F., Ro¨mkens, P.F.A.M., Song, J., Temminghoff, E.J.M., Japenga, J., 2007. Predicting the phytoextraction duration to remediate heavy metal contaminated soils. Water, Air and Soil Pollution 181, 355–371. Lasat, M.M., 2000. Phytoextraction of metals from contaminated soil: a review of plant/soil/metal interaction and assessment of pertinent agronomic issues. Journal of Hazardous Substance Research 2, 1–25. Lombi, E., Zhao, F.J., Dunham, S.J., McGrath, S.P., 2000. Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytologist 145, 11–20. Maxted, A.P., Black, C.R., West, H.M., Crout, N.M.J., McGrath, S.P., Young, S.D., 2007. Phytoextraction of cadmium and zinc from arable soils amended with sewage sludge using Thlaspi caerulescens: development of a predictive model. Environmental Pollution 150, 363–372. McGrath, S.P., Lombi, E., Gray, C.W., Caille, N., Dunham, S.J., Zhao, F.J., 2006. Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environmental Pollution 141, 115– 125. McGrath, S.P., Shen, Z.G., Zhao, F.J., 1997. Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant and Soil 188, 153–159. McGrath, S.P., Zhao, F.J., Lombi, E., 2001. Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant and Soil 232, 207–214. Novozamsky, I., Van Eck, R., Houba, V.J.G., Van der Lee, J.J., 1996. Solubilization of plant tissue with nitric acid-hydrofluoric acid-hydrogen peroxide in a closed system microwave digestor. Communications in Soil Science and Plant Analysis 27, 867–875.
914
G.F. Koopmans et al. / Environmental Pollution 156 (2008) 905–914
Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L.D., Lasat, M.M., Garvin, D.F., Eide, D., Kochian, L.V., 2000. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proceedings of the National Academy of Sciences of the United States of America 97, 4956–4960. Rietra, R.P.J.J., Ro¨mkens, P.F.A.M., Japenga, J., 2004. Cadmium and Zinc in Soil and Arable Crops in the Kempen Region. Report No. 974. Alterra, Wageningen, The Netherlands (in Dutch). Robinson, B.H., Leblanc, M., Petit, D., Brooks, R.R., Kirkman, J.H., Gregg, P.E.H., 1998. The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant and Soil 203, 47–56. Ro¨mkens, P.F.A.M., Zeilmaker, M.J., Rietra, R.P.J.J., Kan, C.A., Van Eijkeren, J.C.H., Van Raamsdonk, L.W.D., Lijzen, J.P.A., 2007. Exposure to and Uptake of Cadmium by Bovine Animals in the Kempen Region: a Model Study. Report No. 1438. Alterra, Wageningen, The Netherlands (in Dutch). Sauve´, S., Hendershot, W., Allen, H.E., 2000. Solid–solution partitioning of metals in contaminated soils: dependence on pH, total metal burden, and organic matter. Environmental Science & Technology 34, 1125–1131. Schwartz, C., Echevarria, G., Morel, J.L., 2003. Phytoextraction of cadmium with Thlaspi caerulescens. Plant and Soil 249, 27–35. Tipping, E., Rieuwerts, J., Pan, G., Ashmore, M.R., Lofts, S., Hill, M.T.R., Farago, M.E., Thornton, I., 2003. The solid–solution partitioning of heavy metals (Cu, Zn, Cd, Pb) in upland soils of England and Wales. Environmental Pollution 125, 213–225.
Van Nevel, L., Mertens, J., Oorts, K., Verheyen, K., 2007. Phytoextraction of metals from soils: how far from practice? Environmental Pollution 150, 34–40. Vellinga, T.V., Andre´, G., 1999. Sixty years of Dutch nitrogen fertiliser experiments, an overview of the effects of soil type, fertiliser input, management and of developments in time. Netherlands Journal of Agricultural Science 47, 215–241. Weng, L., Temminghoff, E.J.M., Van Riemsdijk, W.H., 2001. Contribution of individual sorbents to the control of heavy metal activity in sandy soil. Environmental Science & Technology 35, 4436–4443. Whiting, S.N., Leake, J.R., McGrath, S.P., Baker, A.J.M., 2001. Assessment of Zn mobilization in the rhizosphere of Thlaspi caerulescens by bioassay with nonaccumulator plants and soil extraction. Plant and Soil 237, 147–156. Zhao, F.J., Hamon, R.E., Lombi, E., McLaughlin, M.J., McGrath, S.P., 2002. Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. Journal of Experimental Botany 53, 535–543. Zhao, F.J., Hamon, R.E., McLaughlin, M.J., 2001. Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytologist 151, 613–620. Zhao, F.J., Lombi, E., McGrath, S.P., 2003. Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant and Soil 249, 37–43.