Water, Air, and Soil Pollution

, Volume 206, Issue 1, pp 385–394

Effect of Biosolids and Cd/Pb Interaction on the Growth and Cd Accumulation of Brassica rapa Grown in Cd-Contaminated Soils

Authors

  • Hsuen-Li Chen
    • Department of Environmental EngineeringNational Chung Hsing University
    • Environmental Protection Bureau of Changhua County
    • Department of Post-Modern AgricultureMingDao University
  • Su-Mei Wang
    • Department of Environmental EngineeringNational Chung Hsing University
    • Environmental Protection Bureau of Changhua County
  • Yu-Chen Kuo
    • Department of Environmental EngineeringNational Chung Hsing University
    • Environmental Protection Bureau of Changhua County
  • Chih-Jen Lu
    • Department of Environmental EngineeringNational Chung Hsing University
Article

DOI: 10.1007/s11270-009-0114-9

Cite this article as:
Chen, H., Lai, H., Wang, S. et al. Water Air Soil Pollut (2010) 206: 385. doi:10.1007/s11270-009-0114-9

Abstract

Mixed metals in the cropped lands in central Taiwan contaminated about 230 ha. According to the Soil and Groundwater Protection Remediation Act (SGWR Act) of Taiwan, these lands were restored. However, some grains of paddy rice grown in these remediated soils still contained more than 0.5 mg Cd kg−1, which the Department of Health of Taiwan notified as the maximum allowable Cd content in rice. The suitability of planting edible crops in these soils is now in doubt. Brassica rapa is the crop most often sold in Taiwan's market and is planted in the interval between the first and second stages of planting of paddy rice, especially in central Taiwan where this experiment was conducted. A pot experiment was conducted using soils contaminated artificially with Cd or both Cd and Pb. The soil was then amended with 5% of biosolid and followed by planting of B. rapa. The objectives were to study the effect of biosolid amendment on the soil and the interaction between Cd and Pb on the growth of and Cd accumulation in B. rapa. Experimental result showed that the biomass and the accumulation of Cd by B. rapa were significantly increased in the biosolid-amended soils compared with the control. Lead has a synergistic effect on enhancing the accumulation of Cd by B. rapa grown in artificially Cd-contaminated soils.

Keywords

BiosolidBrassica rapaCadmium (Cd)InteractionLead (Pb)

1 Introduction

Metal-contaminated soils are the result of the combustion of petroleum fuels, application of chemical fertilizers and pesticides, irrigation with illegal wastewater effluent, etc. (Kabata-Pendias and Pendias 2001). The total concentration of cadmium (Cd) in the crust is in the region of 0.3–11 mg kg−1 but mostly below 1 mg kg−1 (Alloway 1995). According to the survey results of the Environmental Protection Administration of Taiwan (EPA) in 1989, the cropped lands which produce harvest in Changhua county, located in central Taiwan, have higher Cd concentration (0.36 mg kg−1) compared to those in other counties. Agricultural irrigation using river water contaminated with metals is the primary reason for the contamination of cropped lands in central Taiwan. Consumption of vegetables grown in the contaminated soil of these lands leads to accumulation or high concentration of metal in edible tissues causing harm to human health. Such negative effects on health could be reduced if these concentrations in the vegetables grown in contaminated soil are significantly lowered (Jarvis et al. 1976). In most of the standards in the world, the tolerance level for Cd concentration in vegetable is less than 0.2 mg kg−1. The maximum level of Cd set by the Joint FAO/WHO Food Standard Program (2002) is 0.05 mg kg−1 for the edible parts of vegetables and 0.2 mg kg−1 for wheat, rice, soybean, and peanut.

In Taiwan, according to the Soil and Groundwater Protection Remediation Act (SGWR Act), the total concentration of metals in soil (digested by aqua regia) was used as the threshold to identify soil contamination. The survey results of Taiwan's EPA in 2002 reported that about 400 ha of cropped lands in Taiwan was contaminated with metals and about 230 and 100 ha of them were in central and northern Taiwan, respectively. Most of the soils contaminated by metals in Taiwan are the result of irrigation with illegal effluent discharged from metal-plating plants in the vicinity. According to the SGWR Act of Taiwan, these lands are regarded as control sites and are required to carry out further remediation to reduce the total metal concentration to below the levels specified by the Soil Pollution Control Standards (SPCS).

The remediation techniques used in Taiwan to treat metals-contaminated soils in control sites include methods for acid washing and soil turnover/dilution. Taiwan's EPA spent about US$ 10 million (2003–2007) to remediate these metals-contaminated lands. The soil turnover/dilution method was the most used method, which mixes the soils in the surface layer and lower layer to reduce the metal concentration because surface soil always has higher concentration compared to the subsoil. While the total amount of metals in soil remains unchanged, soil characteristics manifest change after treatment with this method. Further application of fertilizers or organic materials, however, is necessary for soil fertility to recover (Lai et al. 2007). The threshold of Cd concentration in the grain of paddy rice announced by the Department of Health of the Taiwan is 0.5 mg Cd kg−1. Although the metal concentration in the soil of control sites decreased after turnover/dilution remediation, some paddy rice grown there still showed accumulations in excess of 0.5 mg Cd kg−1 in grains. The Cd concentration accumulated in the tissue of plant was affected by the bioavailability of soil Cd, interaction between soil elements, and the plant species (Alloway 1995; Naidu et al. 1997; Lock and Janssen 2003; Vig et al. 2003; Lai and Chen 2006). Further planting of different types of crops in these contaminated lands treated with soil turnover and dilution method is in doubt.

In Taiwan, biosolids produced by industries such as food processing, leather and tannery, textile, pulp and paper mill, and metal-plating aggregate to about 45 Mg year−1. There were 30 sewage treatment plants in Taiwan and the percentage of public sewage system was about 18% until 2007. The estimated percentage of public sewage will be 33% in 2009 and more than 40 Mg of biosolids will be produced and would need further treatment. Combustion, landfill, and land application are the final disposal methods currently used to treat the biosolids produced from sewage treatment plants (US EPA 1999; Epstein 2003) and, among them, landfill was the method most used in Taiwan. However, alternative methods are needed because the land available in Taiwan for landfill is limited and the leachate may result in soil pollution. Land application of biosolids appears a feasible method in solving this problem in Taiwan.

Many studies have assessed the feasibility of land application of biosolids and investigated the subsequent effect on the growth of plant. Vlamis et al. (1985) continuously applied two types of biosolids for 7 years and planted wheat; no toxic symptoms were found and the yield also increased. The maximum yield was obtained when the application rate for sewage and industrial biosolids were 90 and 45 Mg ha−1, respectively. The average content of nitrogen in the grain of wheat at the end of biosolid application was 1.1% and 3% with sewage biosolids and industrial biosolids, respectively. Bidwell and Dowdy (1987) applied biosolids to land for 6 years continuously and then planted corn for 3 years. Their experimental result showed that the nutrients in the soil after amending with biosolid were sufficient to support the growth of corn, but yield did not improve. However, the enhancing effect of biosolids was also reported by some researchers (Peterson et al. 1994; Gardiner et al. 1995; Brallier et al. 1996). The application of biosolids at 6.6 Mg ha−1 doubled the yield of corn (Peterson et al. 1994). The yield of wheat increased from 1,437 to 2,659 kg ha−1 when farmland was amended with 20 Mg ha−1 of biosolids and reached 2,731 kg ha−1 with treatment of 100 Mg ha−1 (Gardiner et al. 1995). Brallier et al. (1996) planted soybean, cabbage, radish, corn, lettuce, potato, and tomato in a biosolid-amended soil to study its effect on the yield of these crops. They found that a rise in soil pH resulting from the application of biosolid significantly inhibited the uptake of metals by crops. The yield of cabbage, potato, and tomato doubled with the treatment of 500 Mg ha−1 of biosolids. These experimental results showed that the nutrient content in the soil amended with biosolids was sufficient to support the growth of plants.

Application of biosolids to soil had no negative effect on the germination percentage and the growth of roots, and the yield of cabbage significantly increased (Wong et al. 1996; Pichtel and Anderson 1997; Planquart et al. 1999). However, the higher content of salt and soluble metal in the treatment of high application rate of biosolids had a negative effect on the germination, growth, and yield of cabbage (Wong et al. 1996). Because industrial biosolids have higher content of salts and chromium (Cr), the yield of cabbage grown in industrial biosolid-amended soil decreased compared with that in sewage biosolid-amended soil (Wong et al. 2001). The uptake of metal by plants was influenced by both the characteristics of biosolids and the concentration of metal. A relationship was discovered between Cd concentration in 17 biosolids and the uptake by kaoliang (Jing and Logan 1992). Gardiner et al. (1995) found that the uptake of metal by plants increased with an increase in the quantity of biosolids applied.

The interaction between metals has antagonistic or synergistic effect on the accumulation of metal by plants grown in soil contaminated by a combination of metals. The presence of nickel (Ni) and lead (Pb) had enhancing effects on the accumulation of copper (Cu) and zinc (Zn) of winter wheat (Nogales et al. 1997). Soil Cd had enhancing effect on Zn accumulation in the young leaves of lettuce grown in Zn-contaminated soil, but soil Zn has an inhibiting effect on Cd accumulation in the young leaves of lettuce and spinach (McKenna et al. 1993). There was a synergistic effect between Pb and Cd (Hassett et al. 1976; Carlson and Bazzaz 1977). Lead could compete with the exchange sites on the surface of soil colloids with Cd when the soil solution contained both Pb and Cd, especially at higher Cd concentrations (Adriano 1986). Soil Pb thus has an enhancing effect on the accumulation of Cd by plants (Carlson and Rolfe 1979; Adriano 1986; Lai and Chen 2006). Kabata-Pendias and Pendias (2001) summarized the interaction between different metals, but predictions in practice were not easy.

In this study, biosolids taken from a sewage treatment plant in central Taiwan were used. They were applied to artificially Cd- or Cd–Pb-spiked soils that were planted with Brassica rapa to study the effect of Cd/Pb interaction and biosolid amendment on the yield and Cd accumulation of the most consumed crop in Taiwan.

2 Materials and Methods

2.1 Soil and Biosolid Analysis

The soil used in this study was taken from the surface soil (0–20 cm) of a metal-contaminated site in central Taiwan. Soil was air-dried, ground, passed through 10-mesh or 100-mesh sieves, and stored in the plastic vessels for further analysis. The characteristics analyzed included texture (Gee and Bauder 1986), pH value (w/v = 1/1; McLean 1982), organic carbon content (Nelson and Sommers 1982), cation exchange capacity (CEC; Rhoades 1982), water content (Gardner 1986), water-holding capacity (WHC), and total concentration of Cd and Pb (EPA/Taiwan 2002). Artificially spiked Cd- or Cd–Pb-contaminated soils were prepared and used in this study because of the insufficient spatial variation of metals in tested paddy soils. After determining the total Cd and Pb concentrations in the tested soil samples, solutions of Cd(NO3)2·4H2O or Pb(NO3)2 were sprayed to make up their final total concentration (in milligrams per kilogram as individual element) in soils as follows: (a) Cd0, control without applying metal solutions; (b) Cd5, 5 mg Cd kg−1; (c) Cd20, 20 mg Cd kg−1; (d) Pb500, 500 mg Pb kg−1; (e) Pb2,000, 2,000 mg Pb kg−1; (f) Cd5Pb500, 5 mg Cd kg−1 and 500 mg Pb kg−1; and (g) Cd20Pb2,000, 20 mg Cd kg−1 and 2,000 mg Pb kg−1. The concentration of Cd and Pb used was in consultation with the SPCS under the SGWR Act of Taiwan, which specifies different standards for cropped lands (5 mg Cd kg−1 and 500 mg Pb kg−1) and nonfarm lands (20 mg Cd kg−1 and 2,000 mg Pb kg−1). These artificially contaminated soils were subjected to three cycles of wet (50–70% WHC)/dry (air-dried) incubation before the pot experiment to enable the added metals to reach as steady a state as possible (Blaylock et al. 1997).

Biosolids used in this study were obtained from a sewage treatment plant in central Taiwan. After air drying and grinding, they were passed through a 100-mesh sieve and analyzed for the total concentration of Cd and Pb (EPA/Taiwan 2002). Artificially contaminated soils were mixed with or without 5% biosolids. The entire weighed quantity (2.5 kg, dry weight [DW]) of the mixture was added to each pot (16 cm in diameter and 19 cm in height), transported to the phytotron (day/night = 30/25°C) located in MingDao University, and incubated for 1 month. The soil water content was controlled at 50–70% WHC during incubation by adding deionized water every 2–3 days.

2.2 Pot Experiment

Seeds of B. rapa L. (Chinensis Croup cv. Fengshan pakchoi) were planted in contaminated and potted soils to study the growth and accumulation of Cd. Ten seeds of B. rapa were sowed in each pot. After germination, we retained three plants and surplus plants were removed to avoid interference. The soil water content was controlled between 50% and 70% WHC during the pot experiment by adding deionized water every 2–3 days. Shoots of B. rapa were harvested after they grew for 35 days (20 December 2007 to 23 January 2008) and the height and fresh weight (FW) of shoots (above ground parts) determined. They were rinsed with tap water to remove adhered soils and washed with deionized water to avoid interference. The DWs of the shoots were determined after oven drying at 65°C for 72 h. Plant tissues were ground, digested by the H2SO4/H2O2 method (Harmon and Lajtha 1999), and the Cd concentration determined in the digestant with an atomic absorption spectrophotometer (Perkin Elmer Analyst 200).

2.3 Statistics

The variances and the significance of the differences between FW, DW, Cd concentration, total removal of Cd, and bioconcentration factor (BCF) value of the B. rapa grown in (a) various Cd-contaminated soils, (b) soils amended with and without biosolids, and (c) Cd- and Cd–Pb-contaminated soils were analyzed using analysis of variance. Statistical significance was set to p = 0.05.

3 Results and Discussion

3.1 Soil Characteristics

The texture of the tested soil was silty clay (sand 8.80%, silt 50.9%, and clay 40.3%) and its pH values ranged from 6.8 to 7.0. The soil contained 2.52% of organic carbon, its water content was 2.90%, and CEC was 13.2 cmol(+) kg−1. The total concentration values of the eight metals in the soil before artificial spiking were 17.0 mg As kg−1, 0.55 mg Cd kg−1, 54.0 mg Cr kg−1, 54.0 mg Cu kg−1, 103 mg Ni kg−1, 34.0 mg Pb kg−1, 224 mg Zn kg−1, and 0.18 mg Hg kg−1, respectively. The biosolids contained an organic matter of 24.0% and the total nitrogen and total phosphate contents were 6.90% and 1.30%, respectively. The total concentration of As, Cd, and Hg in the biosolids was not detectable, and they were 107 mg Cr kg−1, 182 mg Cu kg−1, 41.9 mg Pb kg−1, 75.0 mg Ni kg−1, and 1,120 mg Zn kg−1, respectively, for the other five metals. Although the biosolids used in this study had relatively higher Zn concentration because it is an essential element, the estimated total Zn concentration in the mixture after amending with 5% of biosolids was approximately 269 mg kg−1 (1,120 mg kg−1 × 5% + 224 mg kg−1 × 95% = 269 mg kg−1). It was still below the SPCS specification (600 mg kg−1) of the SGWR Act for cropped lands. The effect of the metal resulting from the application of 5% of biosolids was thus ignored and is not discussed in this study.

Soils were sampled after the pot experiment and their total concentration of Cd and Pb determined by the method described in Section 2.1; the results are shown in Table 1. For all the treatments of Cd5 and Cd20, the final total concentrations of Cd were at the levels 4.56–5.21 and 15.3–16.9 mg kg−1, which were approximately 91–104% and 77–85% of the target concentration (5 and 20 mg kg−1), respectively. In the treatments of Pb500 and Pb2,000, the final concentrations were about 77–78% and 77–81% of the target concentration (500 and 2,000 mg kg−1), respectively. The final Cd and Pb concentrations after artificial spiking were approximately 10–20% lower than the designed target concentration which revealed that some acceptable losses occurred during the preparation of metal-contaminated soils.
Table 1

The total concentration of Cd and Pb in artificially spiked soils

Treatment

Total Cd concentrationa (mg kg−1)

Total Pb concentrationa (mg kg−1)

Cd0–CK

1.25 ± 0.01

22.4 ± 0.4

Cd5–CK

4.61 ± 0.35

23.5 ± 0.8

Cd20–CK

16.9 ± 1.2

23.3 ± 0.2

Cd5Pb500–CK

4.56 ± 0.09

386 ± 4

Cd20Pb2,000–CK

16.2 ± 0.5

1,625 ± 91

Cd0–BS

1.03 ± 0.05

24.5 ± 0.3

Cd5–BS

5.21 ± 0.11

29.3 ± 0.1

Cd20–BS

16.9 ± 1.0

28.2 ± 0.6

Cd5Pb500–BS

4.40 ± 0.09

394 ± 14

Cd20Pb2,000–BS

15.3 ± 0.4

1,557 ± 25

CK control without applying biosolid, BS applying 5% of biosolid

aMean ± standard deviation; replicate (n) = 3

3.2 Effect of Soil Cd Levels

After growing in Cd5 for 35 days, different Cd concentrations in soil had no significant effect on the FW of B. rapa grown in Cd-contaminated soils (Table 2). The FW increased from 75.0 ± 15.7 g per plant (Cd0) to 99.3 ± 13.8 g per plant and DW increased significantly (p < 0.05) from 1.71 ± 0.16 g per plant (Cd0) to 2.18 ± 0.28 g per plant (1.3-fold). However, the DW of B. rapa grown in Cd20 decreased to 1.60 ± 0.27 g per plant, which was about 90% compared with that grown in Cd0 (Table 2). Excess amounts of Cd have a negative effect on the structure and content of chlorophyll, which may slow down the growth and reduce the yield of plants (Wu et al. 2007). Although the decrease in DW of B. rapa was observed in the soil with Cd20 treatment, the maximum tolerance concentration of soil Cd was not obtained from this study because the change was about 10%.
Table 2

Effect of soil Cd concentration on the growth and Cd accumulation of B. rapa

Treatment

Biomass (g per plant)

Shoot Cd concentration (mg kg−1)

Total removal (μg per plant)

BCF

FW

DW

Cd0

75.0 ± 15.7a

1.71 ± 0.16ab

4.27 ± 0.18b

7.30 ± 0.82b

3.43 ± 0.16a

Cd5

99.3 ± 13.8a

2.19 ± 0.28b

8.80 ± 0.92b

19.3 ± 4.5b

1.99 ± 0.03b

Cd20

78.3 ± 16.2a

1.60 ± 0.27a

36.4 ± 9.8a

56.9 ± 10.9a

2.16 ± 0.61b

Mean ± standard deviation; replicate (n) = 3. Values followed by the same letter within each column are not significantly different at p = 0.05

Results of the pot experiment showed that the Cd concentration in soil had a significant effect on the concentration and total removal of Cd in the shoots of B. rapa (Table 2). After growing in the Cd5 and Cd20 soils for 35 days, the Cd concentration in the shoots rose from 4.27 ± 0.18 mg kg−1 (Cd0) to 8.80 ± 0.92 mg kg−1 (2.06-fold) and 36.4 ± 9.8 mg kg−1 (8.52-fold), respectively. The total removal of Cd also increased from 7.30 ± 0.82 μg per plant (Cd0) to 19.3 ± 4.5 μg per plant (Cd5) and 56.9 ± 10.9 μg per plant (Cd20; Table 2). Because the change of DW in the treatment of Cd20 was slight compared with Cd0, we concluded that B. rapa could tolerate the toxicity of Cd20 (15.3–16.9 mg Cd kg−1 soil). The significant increase in Cd concentration in the shoots of Cd20 soil contributed to the significant increase in total removal compared with that of Cd0. Cadmium concentration in the tissues of the plant increased with that in the external soil; our experiment result is similar to that demonstrated by Gardiner et al. (1995). We concluded that the concentration and total removal of Cd would continue to rise until the Cd concentration in the soil exceeded the tolerance value of B. rapa.

Although soils were artificially spiked with the solutions of Cd or Pb to create the metal-contaminated soils, the final total concentrations of Cd and Pb were approximately 10–20% lower than the target concentrations set (Table 1). BCF was thus used to understand the intricacies of transportation of Cd by B. rapa grown in contaminated soils. Although the Cd concentration in shoots of B. rapa increased with the soil Cd concentration, BCF significantly decreased from 3.43 ± 0.16 (Cd0) to 1.99 ± 0.03 (Cd5) and 2.16 ± 0.61 (Cd20), respectively (Table 2). The result shows that the higher concentration of Cd in soil inhibited the transportation of Cd from soil to the shoot of B. rapa. The Cd concentration in the shoot of B. rapa grown in artificially Cd-contaminated soil doubled when the total Cd concentration in soil exceeded 5 mg kg−1. Because only the edible parts of B. rapa (shoots) were analyzed in this study, we did not understand the intricacies of transportation of Cd from soil to inedible parts (roots). The effect of Cd concentration in soil on the transportation of Cd from soil to root need to be investigated by further studies:
$$ {\text{Bioconcentration factor}}\;\left( {\text{BCF}} \right)\; = \;\;\frac{{{\text{Shoot Cd concentration}}\;\left( {{\text{mg k}}{{\text{g}}^{ - 1}}} \right)\;}}{{{\text{Total soil Cd concentration}}\;\left( {{\text{mg k}}{{\text{g}}^{ - 1}}} \right)}}. $$

3.3 Effect of Biosolids

The application of 5% biosolid had an enhancing effect on increasing the FW and DW (Table 3) of B. rapa for most of the treatments, but was only statistically significant in the treatment of Cd20 because of the larger variations in the other treatments. Biosolids increased the DW of B. rapa grown in Cd0 from 1.71 ± 0.16 to 2.24 ± 0.83 g per plant (1.3-fold). After growing in Cd20 amended with biosolids, their FW and DW increased significantly from 143 ± 28 and 1.60 ± 0.27 to 78.3 ± 16.2 and 2.55 ± 0.17 g per plant, respectively (1.6-fold; p < 0.05). The application of biosolids increased the content of organic matter and nutrients, and the bulk density of the mixture reduced after amending with biosolid (Oberle and Keeney 1994; NRC 1996). The biosolids used in this study had high content of organic carbon (24.0%), total nitrogen (6.90%), and total phosphate (1.30%). The growth of roots and whole plant was thus promoted after biosolid amendment for most of the treatments. Our observation was in agreement with previous studies (Wong et al. 1996; Planquart et al. 1999).
Table 3

Effect of applying biosolid on the growth of B. rapa grown in various Cd-contaminated soils

Treatment

FW (g per plant)

DW (g per plant)

CK

Biosolid

CK

Biosolid

Cd0

75.0 ± 15.7a

95.6 ± 42.3a

1.71 ± 0.16a

2.24 ± 0.83a

Cd5

99.3 ± 13.8a

117 ± 31a

2.19 ± 0.28a

2.04 ± 0.72a

Cd20

78.3 ± 16.2b

143 ± 28a

1.60 ± 0.27b

2.55 ± 0.17a

Mean ± standard deviation; replicate (n) = 3. Values followed by the same letter within each row are not significantly different at p = 0.05

Except for Cd20, the effect of biosolids on the Cd accumulated in the shoot of B. rapa grown in Cd-contaminated soils was not significantly different (Fig. 1). In the Cd5 amended with biosolids, the shoot Cd concentration increased from 8.80 ± 2.52 to 10.8 ± 2.2 mg kg−1 (1.2-fold), and this value significantly increased from 36.4 ± 0.9 to 55.4 ± 11.6 mg kg−1 (1.5-fold) in the Cd20 amended with biosolids (Fig. 1). Because of complex reactions with metals, organic matter has significant effects on reducing the presence of metals in the soil (McBride 1995). According to the research results of previous studies, the application of biosolids could reduce the uptake of Cd by B. rapa grown in Cd-contaminated soils because of the high content of organic matter of biosolids. Our experimental result, however, was not similar to the reports referred. Corey et al. (1987) used the plateau theory to describe the influence of metal concentration on the relationship between the soil in biosolid-amended soil and the plants grown in it. They assumed that the concentration of metal in the plant increased with that in soil amended with biosolids until a plateau was reached. Our experimental result shows that the Cd concentration in the shoot of B. rapa grown in biosolid-amended soil increased with the Cd concentration in the soil. The B. rapa accumulated more Cd in their shoots until a plateau was reached even if the Cd concentration in biosolid-amended soil continued increasing.
https://static-content.springer.com/image/art%3A10.1007%2Fs11270-009-0114-9/MediaObjects/11270_2009_114_Fig1_HTML.gif
Fig. 1

Effect of applying biosolid on the Cd concentration in the shoot of B. rapa grown in various Cd-contaminated soils

Experimental results showed that the application of biosolids has a significant effect on promoting the total removal of Cd from the shoots of B. rapa (Fig. 2). After growing in the Cd5 for 35 days, biosolid treatment improved the total removal of Cd by B. rapa from 19.3 ± 4.5 to 21.1 ± 4.4 μg per plant (1.1-fold). The increase was about 2.5-fold with Cd20 treatment amended with biosolids (Fig. 2). This phenomenon is logical because the DW and Cd concentration of shoot significantly increased after amending with 5% biosolids (Table 3), and thus the total removal increased. Applying biosolids also positively increased the BCF values of B. rapa grown in different Cd-contaminated soils. The BCF value increased from 1.99 ± 0.03 and 2.16 ± 0.61 to 2.07 ± 0.40 and 3.28 ± 0.65 in Cd5 and Cd20, respectively, after amending with biosolids (Fig. 3).
https://static-content.springer.com/image/art%3A10.1007%2Fs11270-009-0114-9/MediaObjects/11270_2009_114_Fig2_HTML.gif
Fig. 2

Effect of applying biosolid on the total removal of Cd by the shoot of B. rapa grown in various Cd-contaminated soils

https://static-content.springer.com/image/art%3A10.1007%2Fs11270-009-0114-9/MediaObjects/11270_2009_114_Fig3_HTML.gif
Fig. 3

Effect of applying biosolid on the BCFs of B. rapa grown in various Cd-contaminated soils

3.4 Interaction Between Cd and Pb

Because wastewater always contains multiple metals in Taiwan, Pb is always accompanied by Cd when paddy soil is contaminated due to the utilization of illegal discharged wastewater for irrigation. Thus, there is higher concentration of Pb in the soil when soil contains higher concentration of Cd. Experimental results showed that the Pb of the soil had a negative effect on the FW and DW of B. rapa grown in Cd-contaminated soil, but its effect was slight and was not statistically significant (Table 4). The DW decreased from 2.18 ± 0.28 g per plant (Cd5) and 1.6 ± 0.27 g per plant (Cd20) to 2.01 ± 0.21 g per plant (Cd5Pb500) and 1.50 ± 0.27 g per plant, respectively.
Table 4

Effect of the interaction between Cd and Pb on the growth and Cd accumulation of B. rapa

Treatment

Biomass (g per plant)

Shoot Cd concentration (mg kg−1)

Total removal (μg per plant)

BCF

FW

DW

Cd5

99.3 ± 13.8a

2.18 ± 0.28a

8.80 ± 0.92a

19.3 ± 4.5a

1.99 ± 0.03a

Cd5Pb500

88.9 ± 4.3a

2.01 ± 0.21a

11.9 ± 2.5a

17.1 ± 16.1a

2.61 ± 0.61a

Cd20

78.3 ± 16.2a

1.60 ± 0.27a

36.4 ± 9.8b

56.9 ± 10.9a

2.16 ± 0.61b

Cd20Pb2,000

83.2 ± 14.1a

1.50 ± 0.27a

102 ± 25a

155 ± 63a

6.29 ± 1.49a

Mean ± standard deviation; replicate (n) = 3. Values followed by the same letter within each column are not significantly different at p = 0.05

The coexistence of Pb in Cd-contaminated soil promoted the accumulation of Cd of the shoots of B. rapa (Table 4). The Cd concentration in the shoot of B. rapa grown in Cd5Pb500 was higher (11.9 ± 2.5 mg kg−1) compared with that in Cd5 (8.80 ± 0.92 mg kg−1; 1.4-fold). The relative increase was more significant (2.8-fold) in the Cd20Pb2,000 treatment soil because of higher plant uptake of Cd from soil. The shoot Cd concentration significantly reached 102 ± 25 mg kg−1 in the treatment of Cd20Pb2,000 compared with that Cd20 (36.4 ± 9.8 mg kg−1; p < 0.05). Cd and Pb appear to compete for the soil of the exchangeable sites on the surface of colloids (Adriano 1986). The existence of Pb in Cd-contaminated soil raises the Cd concentration in the soil solution, increases the availability of Cd, and thus promotes its uptake by plants. The synergistic effect of soil Pb on the accumulation of Cd by plants in this experiment was similar those observed in previous studies (Hassett et al. 1976; Carlson and Rolfe 1979; Wong et al. 1996; Lai and Chen 2006).

Soil Pb also had an enhancing effect on increasing the total removal of Cd and BCF in the shoot of B. rapa grown in Cd-contaminated soils (Table 4). Soil Pb raised the total removal of Cd from 56.9 ± 10.9 μg per plant (Cd20) to 155 ± 62 μg per plant (Cd20Pb2,000; 2.7-fold). For the two Cd concentrations used (Cd5 and Cd20), the change of BCF value was more drastic in the treatment with the higher concentration. The BCF rose from 1.99 ± 0.03 (Cd5) to 2.61 ± 0.61 (Cd5Pb500) and significantly increased from 2.16 ± 0.61 (Cd20) to 6.29 ± 1.49 (Cd20Pb2,000; p < 0.05), respectively.

3.5 Removal of Soil Cd by B. rapa

The uptake capacity of B. rapa was of a grade higher than of other vegetables. Previous studies attempted to use the total Cd in soil, biomass, and Cd concentrations to predict the time needed to remove the Cd in contaminated soil in an ideal situation. This calculation was used in this study, although some of the assumptions were unreasonable, which included the availability of soil Cd might decrease with time, the uptake of Cd was not linear, and B. rapa being an edible crop and is not a suitable phytoextraction plant. The time needed for B. rapa to remove the Cd in contaminated soil is approximately 39 and 50 years for Cd5 and Cd20, respectively, if we planted six times a year. The application of biosolids reduced the time needed for decontamination to 41 years (Cd5) and 20 years (Cd20).

The normal content of Cd in different plants was at the level 0.01–0.1 mg kg−1 (Kabata-Pendias and Pendias 2001). After growing for 35 days, the Cd concentration in the shoots of B. rapa was 4.27 ± 0.18 mg kg−1 (Cd0), 8.80 ± 0.92 mg kg−1 (Cd5), 11.9 ± 2.5 mg kg−1 (Cd5Pb500), 36.4 ± 9.8 mg kg−1 (Cd20), and 102 ± 25 mg kg−1 (Cd20Pb2,000). The daily uptake of Cd is about 32.1 μg per person and the limiting value is at the level of 48–60 μg per person if the body weight is 60 kg per person (Joint FAO/WHO Food Standards 2002). The Department of Health of Taiwan has suggested that an adult consumes 300 g of vegetable a day. If an adult consumed only the B. rapa grown in this study in place of other vegetables, the daily Cd uptake would reach 85.4 μg person−1 day−1 (Cd0), 176 μg person−1 day−1 (Cd5), and 655 μg person−1 day−1 (Cd20). These values are all in excess of the limiting value notified by the Department of Health of Taiwan. Therefore, consumption of B rapa harvested from a Cd-contaminated site is not recommended.

4 Conclusion

Experimental results showed that the concentration and total amounts of Cd contained in the shoots of B. rapa increased with the Cd concentration in the external soil. A slightly negative effect occurred on the biomass when the concentration of total Cd in soil was 20 mg kg−1. The application of 5% biosolids had a positive effect on increasing the biomass of B. rapa grown in Cd-contaminated soils. The concentration, total removal, and BCF of Cd significantly increased in the biosolid-amended soils. Lead has a synergistic effect on enhancing the uptake of Cd by B. rapa and thus results in slightly decreasing the biomass, but is not statistically significant. The Cd concentration in the shoots of B. rapa grown in Cd-contaminated soil was higher than 4.27 ± 0.18 mg kg−1 even for that grown in Cd0 (total Cd concentration is 1.25 mg kg−1). Consumption of 300 g a day of B. rapa planted in these contaminated soils is harmful because the uptake exceeds 85.4 μg Cd day−1, which exceeds the notified limiting value of the Department of Health of Taiwan.

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© Springer Science+Business Media B.V. 2009