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Accumulation of cadmium in the edible parts of six vegetable species grown in Cd-contaminated soils
Journal of Environmental Management 90 (2009) 1117–1122
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Accumulation of cadmium in the edible parts of six vegetable species grown in Cd-contaminated soils Yong Yang, Fu-Suo Zhang, Hua-Fen Li*, Rong-Feng Jiang College of Resources and Environmental Sciences, China Agricultural University, 2 YuanMingYuan West Road, HaiDian District, Beijing 100094, PR China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 September 2007 Received in revised form 8 April 2008 Accepted 6 May 2008 Available online 26 June 2008
Species difference in Cd accumulation is important for selection of agronomic technologies aimed at producing low-Cd vegetables. Six vegetable species (Chinese leek, pakchoi, carrot, radish, tomato and cucumber) were grown in pot and field experiments to study the accumulation of Cd under different conditions. In the field trial (Cd 2.55 mg kg1), Cd concentrations in the edible parts ranged from 0.01 to 0.1 mg kg1 and were below the permissible limits (0.2 mg kg1 for pakchoi and leek; 0.1 mg kg1 for carrot and radish; 0.05 mg kg1 for cucumber and tomato), but exceeded the limit in pakchoi, Chinese leek, carrot and tomato at a Cd addition level of 2.0 mg kg1. Plant Cd concentrations increased linearly with the increasing concentration of Cd added to the soil, with the slope of the regression lines varying by 28-fold among the six species. The bioconcentration factor (BCF) varied substantially, and was much higher in the pot experiment than in the field trial. It is concluded that the vegetable species differed markedly in the Cd accumulation and species performed consistently under different growth conditions. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Cadmium Threshold Vegetable species Bioconcentration factor Risk assessment
1. Introduction There is increasing concern regarding food safety due to environmental pollution. Cadmium (Cd) is a non-essential metal element that is believed to cause damage even at very low concentrations and can be taken up by crops easily (Wagner, 1993). Soils may be contaminated with Cd due to the disposal of municipal and industrial wastes, irrigation with sewage effluent, application of phosphorous fertilizers, and atmospheric deposition (Harrison and Chirgawi, 1989; Jackson and Alloway, 1991; Kim et al., 1988). It is well known that cadmium can enter into the food chain via plant uptake from contaminated soils. Toxicity of ingested Cd is an important issue for human health. Vegetables are a good source of vitamins, minerals and fibers. However, many studies have shown that some garden vegetables are capable of accumulating relatively high levels of Cd from the soil (Alloway et al., 1988; Bahemuka and Mubofu, 1999; Cobb et al., 2000; Khan and Frankland, 1983), and accumulation of Cd in plant tissues is influenced by the availability of Cd in the soil and Cd–Zn interaction (Ahumada et al., 1999; Alloway et al., 1990; Brown et al., 1998; Hart et al., 2002). Hart et al. (2002) found that high-Zn treatment decreased the accumulation of Cd in wheat seedlings. Ingestion of high-Cd-containing crops may contribute a substantial amount of Cd to the human diet (Wagner, 1993). People who
consume vegetables grown in Cd-contaminated soils in the urban areas are at risk of an elevated Cd exposure (Datta and Young, 2005; Hough et al., 2004). China has undergone rapid industrialization and urbanization over the last two decades. As a consequence, environmental pollution has become an important issue that affects public health. In recent years, Cd contamination of soils, food crops and vegetables have been reported frequently (Li et al., 2006; Wang et al., 2005). Farmlands around cities are often used for growing vegetables, and are particularly vulnerable to metal contamination. Thus a more pragmatic solution is to assess the risk of Cd concentration exceeding the national limits in different vegetables, and advise farmers accordingly. This requires knowledge of Cd accumulation of different vegetable species and cultivars, as well as soil factors that control Cd bioavailability to plants. A better understanding of species difference in Cd accumulation is important for selection of agronomic technologies aimed at producing low Cd vegetables. The objectives of the present study were to determine the Cd accumulation in the edible parts of six common vegetable species in the Beijing area, and to compare the levels of Cd accumulation in pot experiment with Cd-spiked soil and those under field conditions. 2. Materials and methods 2.1. Pot experiment
* Corresponding author. Tel.: þ86 10 6273 1165; fax: þ86 10 6273 1016. E-mail address: [email protected] (H.-F. Li). 0301-4797/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvman.2008.05.004
A pot experiment was conducted with six vegetable species that are most commonly consumed by the population in Beijing (Table 1)
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Table 1 Species of the selected vegetables and the sowing time Vegetable species
Cultivar
Sowing time (growth period, weeks) in the pot experiment
Sowing time (growth period, weeks) in the field trial
Chinese leek (Allium tuberosum Rottl. ex Spr.) Pakchoi (Brassica rapa L. spp. Chinenesis) Pakchoi (Brassica rapa L. spp. Chinenesis) Carrot (Daucus carota var. sativa DC.) Radish (Raphanus sativus L.) Cucumber (Cucumis sativus L.) Tomato (Lycopersicon esculentum Mill.)
Youxi 791 Xinchun Wuyueman Juhong 1 Huaye Zhongnong 8 Jiafen 16
April 14 (13) March 25 (9) March 25 (9) April 14 (13) April 14 (13) April 28 (15) April 28 (15)
March 15 March 15 March 15 March 15 March 15 March 15 March 15
(Ministry of Agriculture of the People’s Republic of China, 2005). The soil used in the experiment was a topsoil (0–20 cm) collected from an uncontaminated vegetable field of China Agricultural University, Haidian district of Beijing, China. The soil had the following characteristics: pH (in H2O) 7.6, organic matter 1.93%, CEC 20.1 cmol kg1, total Cd 0.07 mg kg1 and 0.005 mol L1 DTPA-extractable Cd 0.01 mg kg1. The soil was air-dried, passed through a 5-mm sieve, and spiked with different Cd doses of 0, 0.3, 0.5, 1.0, 1.5 and 2.0 mg kg1 soil by spraying a CdSO4 solution. Soil moisture content was raised to 60% of the water holding capacity and left to equilibrate for 2 weeks. Eight kilograms of the prepared soil were placed in each porcelain pot for growing carrot, radish, cucumber and tomato, and 4 kgfor pakchoi cultivars (Xinchun and Wuyueman) and Chinese leek. Each Cd treatment was replicated in three pots for each vegetable species. The doses of N (in urea), P (in KH2PO4), and K (in K2SO4) were equal for all treatments in the pot experiment: 0.30 g N, 0.20 g P, and 0.30 g K kg1 soil. The pots were randomly arranged inside a netted greenhouse. Seeds were sown directly to the soil pots at the times shown in Table 1, which coincided with the normal growing season for each vegetable. Following emergence the number of seedlings was thinned to six per pot for pakchoi cultivars, 20 for Chinese leek, three for carrot, and one for radish, cucumber and tomato. During the experimental period, tap water was added to compensate for evaporation and transpiration and soil moisture content was maintained at approximately 60% of water holding capacity. The edible parts of the vegetables were harvested at a time that was appropriate for each species. 2.2. Field experiment The experimental field was located at DaXing district (latitude N 39 410, longitude E 116 360 ) on the outskirts of Beijing. The vegetables planted in this field included pakchoi, celery and tomato. Typically, vegetables are grown inside greenhouses (80 m 7 m) that are constructed with clay walls and covered with polyethylene film. One greenhouse was selected for this study, which had a 15year cropping history of continuous vegetable production. Cadmium accumulation in the soil of greenhouse is mainly due to the application of manure and fertilizer with Cd for long time. Soil in the selected greenhouse had the following characteristics: pH (H2O) 7.29, organic matter 2.41%, total Cd 2.55 mg kg1 and DTPAextractable Cd 0.91 mg kg1. The same vegetable species as those used in the pot experiment (Table 1) were grown in the field trial. Conventional fertilization and irrigation practices were adopted in this study. Before planting, 35 kg compound fertilizer, 1000 kg chicken manure and 1000 kg cattle manure were applied to the soil inside the greenhouse. For the convenience of management, the greenhouse area was divided into three parts for growing leafy vegetables, rootstalk vegetables and fruit vegetables. Each vegetable species was grown in four replicate plots that were arranged randomly. The plot sizes were 6, 9 and 12 m2
(17) (8) (8) (12) (12) (17) (17)
for leafy vegetables, rootstalk vegetables and fruit vegetables, respectively. Seeds of leafy vegetables, rootstalk vegetables and cucumber were sown directly onto the seedbeds. For tomato, 4-week-old seedlings were transplanted to the seedbeds. Plant density was determined as follows: 33 104 plants ha1 for leaf vegetables, 4 104 plants ha1 for fruit vegetables, 9 104 and 5 104 plants ha1 for carrot and radish, respectively. The edible parts of the six vegetables were harvested at times appropriate for each species (Table 1). 2.3. Chemical analysis The collected vegetable samples were washed in deionized water, and homogenized in a blender. Fresh sub samples were weighed and digested by HNO3 and HClO4 (4:1). Soil samples were air dried and ground, and digested by HCl/HNO3/HClO4/HF (State Environmental Protection Administration of China, 1997). Total Cd concentrations in soil and vegetable were determined by an atomic absorption spectrophotometer with graphite furnace atomization (GFAAS). Blanks and standard reference materials (Tomato Leaves NIST 1572 and Soil ESS-4 GSBZ50014-88) were included for quality assurance. The recovery ratios were from 89% to 116% throughout the analysis procedures. 2.4. Data analysis The significance of differences between the means of the treatments was evaluated by one-way analysis of variance followed by LSD tests. Linear regression analysis was performed to establish the relationships between the Cd concentrations in the edible parts of vegetables and the Cd concentrations in soil. Statistical analysis were performed with the software SAS (version 8.02). 3. Results and discussion 3.1. Pot experiment In the pot experiment, the growth of all vegetables was not affected by the addition of Cd, because of the relatively low doses of Cd additions. Fig. 1 shows the Cd concentrations in the edible parts of vegetables expressed on a fresh weight basis, because the national allowable limits for Cd are also based on the fresh weight. Cd concentration in vegetables increased linearly with the increasing concentration of Cd added to the soil (Fig. 1). The regression slopes were significantly different (P < 0.01). The slope of the regression lines varied by 28 fold among the six vegetables and followed the order of carrot > pakchoi (Wuyueman) > pakchoi (Xinchun) > Chinese leek > tomato > radish > cucumber (Table 2), indicating large differences in the patterns of Cd accumulation. Some studies have also indicated a linear relationship between the concentration of trace elements in soils and that in crops (Chen, 1991; Ni et al., 2002).
Y. Yang et al. / Journal of Environmental Management 90 (2009) 1117–1122
Cd concentration in the edible parts (mg kg-1 FW)
1.6 Chinese leek
1.6
Xinchun
Wuyueman
1.2
Carrot Radish
1.2
0.8
0.8
0.4
0.4
0.0
1119
0.0 0.0
0.5
1.0
1.5 1.6 1.2
2.0
2.5
0.0
0.5
1.0
1.5
2.0
2.5
Tomato Cucumber
0.8 0.4 0.0 0.0
0.5
1.0
1.5
2.0
2.5
Cd concentration added in soil (mg kg-1) Fig. 1. Cd concentrations in the edible parts of vegetables grown in Cd-spiked soil. Vertical bars represent means SD of three replicates and lines are the fitted linear regression lines.
According to the China environmental quality standard for soils (State Environmental Protection Administration of China, 1995), Cd limits for the soils used for vegetable production are 0.3 and 0.6 mg kg1 for pH < 7.5 and pH > 7.5, respectively. At a Cd level of 0.6 mg kg1, Cd concentrations in six vegetables ranged from 0.02 to 0.43 mg kg1, representing a 21-fold variation. At this level of Cd addition, the national allowable limits of Cd in vegetables (Ministry of Health of the People’s Republic of China and Standardization Administration of China, 2005, Maximum levels of contaminants in foods, 0.2 mg kg1 for pakchoi and leek; 0.1 mg kg1 for carrot and radish; 0.05 mg kg1 for cucumber and tomato) were exceeded in pakchoi (Wuyueman), carrot and tomato. In general, carrot and leafy vegetables accumulate higher Cd concentrations in their edible parts than radish and fruit vegetables. Plants have been shown to vary greatly in metal accumulation from the soil (Cui et al., 2004; Freedman and Hutchinson, 1980; Harrison and Chirgawi, 1989; Kurz et al., 1999; Wang et al., 2006). The results from the present study also showed a large variation among vegetables in Cd concentration, reflecting variation in Cd uptake. In this study, leafy vegetables and carrot had a high risk for Cd accumulation in their edible parts compared with fruit vegetables. Our results are in agreement with previous findings that leafy vegetables and root crops generally have higher Cd concentrations than fruits or seeds (Jinadasa et al., 1997; Lund et al., 1981). Most plant species tend to sequester metals in their roots, with only small amounts of metals being translocated to the above-ground
parts (Kim et al., 1988; Moreno-Caselles et al., 2000). Cataldo et al. (1981) observed that Cd was strongly retained by soybean roots, with only 2% of the accumulated Cd being transported to leaves. Cd accumulation in the vegetables was significantly affected by species. Fruit vegetables appear to be relatively low accumulators of Cd in their edible parts and so would be more suitable species to grow, whereas leafy vegetables tend to accumulate more Cd in leaves. Interestingly, carrot accumulated greater concentration than radish in taproot and appeared to be relatively high accumulator of Cd. Alexander et al. (2006) also identified carrot as intermediate Cd accumulator while French bean and pea were relatively low accumulator and lettuce and spinach were the high accumulator. In addition, two varieties of pakchoi also showed a significant difference in Cd accumulation (P < 0.05). Some similar results had also been found in potato (McLaughlin et al., 1994), lettuce (John and van Laerhoven, 1976), carrot and pea (Alexander et al., 2006). Because linear regression explained a large percentage of the variance (>74%), the regression equation obtained (Table 2) could be used to estimate the threshold of Cd in the tested soil above which the limit for vegetable Cd concentration is breached. The calculated threshold values (Table 2) were below the environmental quality standard for soils (0.6 mg kg1) for pakchoi (Wuyueman), carrot and tomato, suggesting that these vegetable species are at a higher risk of exceeding the national allowable limits. In contrast, the calculated threshold values were higher than
Table 2 Relationship between Cd concentration in the edible parts and that in soil (n ¼ 6), the calculated thresholds of Cd in soil from pot experiment, and bioconcentration factor (BCF) Vegetable species
Regression equation
r2-value
Cd threshold in soil (mg kg1)
BCF in pot experiment
BCF in field trial
Chinese leek Pakchoi (Xinchun) Pakchoi (Wuyueman) Carrot Radish Cucumber Tomato
y ¼ 0.1237x þ 0.0239 y ¼ 0.3063x 0.0233 y ¼ 0.4225x þ 0.003 y ¼ 0.6165x þ 0.0132 y ¼ 0.0357x þ 0.0031 y ¼ 0.0221x þ 0.0031 y ¼ 0.0519x þ 0.0251
0.9419** 0.9750** 0.9655** 0.9954** 0.8997** 0.7365* 0.8629**
1.42 0.73 0.47 0.14 2.71 2.12 0.48
0.15 0.24 0.37 0.62 0.04 0.03 0.09
0.032 0.030 0.039 0.030 0.009 0.004 0.005
**P < 0.01, *P < 0.05.
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Concentration of Cd was generally low in the field study even the treated soil became strongly contaminated with metals (Dudka et al., 1996). Some studies indicated that the aging of Cd in the soil would decrease the bioavailability of heavy metals and reduce the Cd content in the edible part (Gray et al., 1998; Martinez and Motto, 2000). Martinez and Motto (2000) reported that the transformation of heavy metals added as single solutions in mineral soils could become equilibrated after 40 days of incubation. Gray et al. (1998) also found that the proportion of Cd desorbed was decreased by increasing initial contact time. Similarly, Hooda and Alloway (1993) showed that ryegrass accumulated much more Cd when grown on soils spiked with Cd(NO3)2 than on the sewage sludge treated soils. Furthermore, Cd–Zn antagonism should be taken into account for the lower accumulation of Cd in the field experiment. Under ‘‘natural’’ conditions, Cd contamination in most cases is accompanied by Zn contamination. Some researches have proved the enhanced Zn in soils induced reduction in accumulation of Cd (Hart et al., 2002; Podar et al., 2004). However, the order of accumulation of Cd by selected species of vegetables in the pot study was consistent with that in the field study. It is, therefore, possible to select vegetable species that have a lower risk of Cd transfer from contaminated soils. The dose–response equations were derived from plant uptake experiments that were carried out in pot trials amended with soluble cadmium salts. In most cases, the soil metal limits are lower due to the high bioavailability of metals in soil. It is common conception nowadays that the total concentrations of metals in soils are not a good indicator of bioavailability, or a good tool for potential risk assessment, due to the different and complex distribution patterns of metals among various chemical species or solid phases (Brown et al., 1998; Chen et al., 1996; Jackson and Alloway, 1991). Hence the bioavailability of metal to plants should be taken into account as the basis of soil environmental quality criteria and risk assessment. Both Cd uptake and Cd BCF were greater in the pot experiments, also indicating that the Cd accumulation in the edible parts depended on bioavailable Cd amount rather than the total concentration. Relative lower BCF values of vegetables were also found in another field investigation (Wang et al., 2006). The BCF mean values for leek, pakchoi (Xinchun), pakchoi (Wuyueman), carrot, radish, cucumber, tomato in pot experiment were about 4, 7, 9, 20, 3, 6 and 17 times higher than those in the field trial, respectively (Table 2). There were no apparent differences among Chinese leek, pakchoi and carrot in the BCF values. The efficiency of Cd uptake, measured by BCF, varied over a wide range and depended strongly on the vegetable species. The Joint FAO/WHO Expert Committee on Food Additives (WHO, 2001) proposed a provisional tolerable weekly intake (PTWI) of 7 mg Cd kg1 body weight per week for adults, equivalent to 60 mg Cd per day for an average adult weighing 60 kg. Using average vegetable consumption data (Ministry of Agriculture of the People’s Republic of China, 2005; National Bureau of Statistics of China,
the environmental quality standard for soils for Chinese leek, pakchoi (Xinchun), radish and cucumber, indicating that they are at a lower risk. These calculations are based on the assumption that soil Cd has a bioavailability as high as that of the added Cd salt, which is generally not the case (see below) and should be regarded as the worst-case scenario in a risk assessment. The bioconcentration factor (BCF), defined as the ratio of metal concentration in the edible part to the total metal concentration in soil, was used to evaluate the transfer potential of a metal from soil to plant (Alloway et al., 1990; Chumbley and Unwin, 1982; Harrison and Chirgawi, 1989), which is a function of the properties of the metal itself, the soil properties and the genotype of the plant. The BCF values on the basis of fresh weight varied among vegetables, indicating the difference in the accumulation ability of Cd for six vegetables (Table 2). Carrot had the highest BCF value (0.62), which was about 20 times higher than that of cucumber in the pot experiment. To explain whether differences in the Cd concentration could be due to different water contents of the vegetables, Cd concentrations are also expressed on a dry weight basis (Table 3). Higher Cd concentrations on the dry weight basis were also observed in carrot and leafy vegetables. However, the highest Cd concentration on the dry weight basis was found in pakchoi (Wuyueman), whereas carrot had the highest Cd concentration on the fresh weight basis. A similar ranking in Cd concentration for the fresh weight basis and dry weight basis was found for other vegetables. 3.2. Field trial In the field trial, the Cd concentrations in the edible parts of the six vegetables ranged from 0.01 to 0.1 mg kg1, which were below the national allowable limits (Fig. 2), even though the soil had a substantially elevated concentration of Cd (2.55 mg kg1). Higher Cd concentrations were found in Chinese leek, pakchoi (Xinchun and Wuyueman) and carrot than in radish, cucumber and tomato. Despite the much lower concentrations recorded in the field trial than in the pot experiment, the ranking of the six vegetables in terms of Cd accumulation was similar in the two experiments, indicating that species performed consistently under different growth conditions. Furthermore, the vegetable species showed a similar ranking in Cd concentration based on the fresh weight and on the dry weight (Fig. 2). The Cd concentrations in the edible parts of vegetables grown in Cd-spiked soil in the pot experiment and in the field Cd-contaminated soil showed large differences. The Cd concentrations were above the allowable limits for leafy vegetables and carrot grown in 2.0 mg kg1 Cd-spiked soil, but were below the limit in the field experiment with a soil Cd of 2.55 mg kg1. It is clear that the bioavailability of Cd in the soil in the field trial was much lower than that of the freshly spiked Cd in the pot experiment. Bioavailability of Cd in a field contaminated soil was about 4–18% of that of the freshly added Cd in the pot experiment.
Table 3 Cd concentrations in the edible parts of vegetables grown in Cd-amended soil (mg kg1 dry weight) Vegetable species
Chinese leek Pakchoi (Xinchun) Pakchoi (Wuyueman) Carrot Radish Cucumber Tomato
Added soil Cd (mg kg1) 0.0
0.3
0.6
1.0
1.5
2.0
0.05 0.01 0.10 0.05 0.38 0.12 0.15 0.27 0.01 0.02 0.08 0.08 0.05 0.01
0.48 0.08 0.63 0.42 2.07 1.15 1.61 0.14 0.19 0.05 0.05 0.02 0.63 0.17
1.06 0.17 1.79 0.70 4.63 1.24 2.51 0.61 0.48 0.25 0.24 0.06 0.87 0.15
1.48 0.18 3.33 0.56 5.02 1.30 3.81 0.42 0.82 0.49 0.44 0.02 0.94 0.06
1.63 0.23 4.30 0.88 5.81 0.13 6.00 2.14 0.66 0.30 0.78 0.10 1.26 0.06
1.88 0.07 6.53 1.58 10.87 0.94 7.02 1.16 1.00 0.15 0.55 0.16 1.48 0.35
Values are presented as mean SD of three replicates.
Y. Yang et al. / Journal of Environmental Management 90 (2009) 1117–1122
a
0.15
0.09 0.06 0.03
at o To
m
be uc um
ad R
r
is h
t ro ar C
C
hi
ne
Xi n
se
le
ch un W uy ue m an
ek
0
C
b
2.0 1.6 1.2 0.8 0.4
o at m To
um uc C
R
ad
is
be
r
h
t ro ar
m ue uy W
C
n hu Xi
nc
le se C
hi
ne
an
0.0 ek
Cd concentration in the edible parts (mg kg-1)
0.12
Fig. 2. Cd concentrations in the edible parts of vegetables grown in Cd-contaminated soil on the fresh weight (a) and dry weight (b). Vertical bars represent means SD of four replicates.
2005) and the Cd concentrations in the field trial, the average Cd intake from consumption of the six vegetables was estimated to be 10 mg day1 per person, which accounts for 16.7% of the PTWI. This is likely to represent the worst case scenario, because only a relatively small proportion of vegetable farmland in Beijing is contaminated with Cd. 4. Conclusions The present study showed a large variation among the six major vegetable species in the accumulation of Cd. We obtained the same results from the pot experiment and the field trial. Furthermore, the bioavailability of Cd was much lower in the field contaminated soil than in the artificially contaminated soil used in the pot experiment. The study provided data on the Cd accumulation of six major vegetable species. The results showed that selection of vegetables with low Cd uptake on contaminated soil could contribute to reducing Cd transfer from soil to food crops, and subsequently human Cd intake. Acknowledgments The authors are grateful to the financial support from the key project of Ministry of Agriculture, China (Project number: 2003Z53), and from the vegetable technological project of Beijing Agricultural Bureau. H.-F L. was supported by China Scholarship Council for a study visit to Rothamsted Research. We thank Dr. Fangjie Zhao for his helpful comments and polishing of the English in the manuscript during the study in Rothamsted Research. References Ahumada, I., Mendoza, J., Navarrete, E., Ascar, L., 1999. Sequential extraction of heavy metals in soils irrigated with wastewater. Communications in Soil Science and Plant Analysis 30, 1507–1519. Alexander, P.D., Alloway, B.J., Dourado, A.M., 2006. Genotypic variations in the accumulation of Cd, Cu, Pb and Zn exhibited by six commonly grown vegetables. Environmental Pollution 144, 736–745.
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Accumulation of cadmium in the edible parts of six vegetable species grown in Cd-contaminated soils Yong Yang, Fu-Suo Zhang, Hua-Fen Li*, Rong-Feng Jiang College of Resources and Environmental Sciences, China Agricultural University, 2 YuanMingYuan West Road, HaiDian District, Beijing 100094, PR China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 September 2007 Received in revised form 8 April 2008 Accepted 6 May 2008 Available online 26 June 2008
Species difference in Cd accumulation is important for selection of agronomic technologies aimed at producing low-Cd vegetables. Six vegetable species (Chinese leek, pakchoi, carrot, radish, tomato and cucumber) were grown in pot and field experiments to study the accumulation of Cd under different conditions. In the field trial (Cd 2.55 mg kg1), Cd concentrations in the edible parts ranged from 0.01 to 0.1 mg kg1 and were below the permissible limits (0.2 mg kg1 for pakchoi and leek; 0.1 mg kg1 for carrot and radish; 0.05 mg kg1 for cucumber and tomato), but exceeded the limit in pakchoi, Chinese leek, carrot and tomato at a Cd addition level of 2.0 mg kg1. Plant Cd concentrations increased linearly with the increasing concentration of Cd added to the soil, with the slope of the regression lines varying by 28-fold among the six species. The bioconcentration factor (BCF) varied substantially, and was much higher in the pot experiment than in the field trial. It is concluded that the vegetable species differed markedly in the Cd accumulation and species performed consistently under different growth conditions. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Cadmium Threshold Vegetable species Bioconcentration factor Risk assessment
1. Introduction There is increasing concern regarding food safety due to environmental pollution. Cadmium (Cd) is a non-essential metal element that is believed to cause damage even at very low concentrations and can be taken up by crops easily (Wagner, 1993). Soils may be contaminated with Cd due to the disposal of municipal and industrial wastes, irrigation with sewage effluent, application of phosphorous fertilizers, and atmospheric deposition (Harrison and Chirgawi, 1989; Jackson and Alloway, 1991; Kim et al., 1988). It is well known that cadmium can enter into the food chain via plant uptake from contaminated soils. Toxicity of ingested Cd is an important issue for human health. Vegetables are a good source of vitamins, minerals and fibers. However, many studies have shown that some garden vegetables are capable of accumulating relatively high levels of Cd from the soil (Alloway et al., 1988; Bahemuka and Mubofu, 1999; Cobb et al., 2000; Khan and Frankland, 1983), and accumulation of Cd in plant tissues is influenced by the availability of Cd in the soil and Cd–Zn interaction (Ahumada et al., 1999; Alloway et al., 1990; Brown et al., 1998; Hart et al., 2002). Hart et al. (2002) found that high-Zn treatment decreased the accumulation of Cd in wheat seedlings. Ingestion of high-Cd-containing crops may contribute a substantial amount of Cd to the human diet (Wagner, 1993). People who
consume vegetables grown in Cd-contaminated soils in the urban areas are at risk of an elevated Cd exposure (Datta and Young, 2005; Hough et al., 2004). China has undergone rapid industrialization and urbanization over the last two decades. As a consequence, environmental pollution has become an important issue that affects public health. In recent years, Cd contamination of soils, food crops and vegetables have been reported frequently (Li et al., 2006; Wang et al., 2005). Farmlands around cities are often used for growing vegetables, and are particularly vulnerable to metal contamination. Thus a more pragmatic solution is to assess the risk of Cd concentration exceeding the national limits in different vegetables, and advise farmers accordingly. This requires knowledge of Cd accumulation of different vegetable species and cultivars, as well as soil factors that control Cd bioavailability to plants. A better understanding of species difference in Cd accumulation is important for selection of agronomic technologies aimed at producing low Cd vegetables. The objectives of the present study were to determine the Cd accumulation in the edible parts of six common vegetable species in the Beijing area, and to compare the levels of Cd accumulation in pot experiment with Cd-spiked soil and those under field conditions. 2. Materials and methods 2.1. Pot experiment
* Corresponding author. Tel.: þ86 10 6273 1165; fax: þ86 10 6273 1016. E-mail address: [email protected] (H.-F. Li). 0301-4797/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvman.2008.05.004
A pot experiment was conducted with six vegetable species that are most commonly consumed by the population in Beijing (Table 1)
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Table 1 Species of the selected vegetables and the sowing time Vegetable species
Cultivar
Sowing time (growth period, weeks) in the pot experiment
Sowing time (growth period, weeks) in the field trial
Chinese leek (Allium tuberosum Rottl. ex Spr.) Pakchoi (Brassica rapa L. spp. Chinenesis) Pakchoi (Brassica rapa L. spp. Chinenesis) Carrot (Daucus carota var. sativa DC.) Radish (Raphanus sativus L.) Cucumber (Cucumis sativus L.) Tomato (Lycopersicon esculentum Mill.)
Youxi 791 Xinchun Wuyueman Juhong 1 Huaye Zhongnong 8 Jiafen 16
April 14 (13) March 25 (9) March 25 (9) April 14 (13) April 14 (13) April 28 (15) April 28 (15)
March 15 March 15 March 15 March 15 March 15 March 15 March 15
(Ministry of Agriculture of the People’s Republic of China, 2005). The soil used in the experiment was a topsoil (0–20 cm) collected from an uncontaminated vegetable field of China Agricultural University, Haidian district of Beijing, China. The soil had the following characteristics: pH (in H2O) 7.6, organic matter 1.93%, CEC 20.1 cmol kg1, total Cd 0.07 mg kg1 and 0.005 mol L1 DTPA-extractable Cd 0.01 mg kg1. The soil was air-dried, passed through a 5-mm sieve, and spiked with different Cd doses of 0, 0.3, 0.5, 1.0, 1.5 and 2.0 mg kg1 soil by spraying a CdSO4 solution. Soil moisture content was raised to 60% of the water holding capacity and left to equilibrate for 2 weeks. Eight kilograms of the prepared soil were placed in each porcelain pot for growing carrot, radish, cucumber and tomato, and 4 kgfor pakchoi cultivars (Xinchun and Wuyueman) and Chinese leek. Each Cd treatment was replicated in three pots for each vegetable species. The doses of N (in urea), P (in KH2PO4), and K (in K2SO4) were equal for all treatments in the pot experiment: 0.30 g N, 0.20 g P, and 0.30 g K kg1 soil. The pots were randomly arranged inside a netted greenhouse. Seeds were sown directly to the soil pots at the times shown in Table 1, which coincided with the normal growing season for each vegetable. Following emergence the number of seedlings was thinned to six per pot for pakchoi cultivars, 20 for Chinese leek, three for carrot, and one for radish, cucumber and tomato. During the experimental period, tap water was added to compensate for evaporation and transpiration and soil moisture content was maintained at approximately 60% of water holding capacity. The edible parts of the vegetables were harvested at a time that was appropriate for each species. 2.2. Field experiment The experimental field was located at DaXing district (latitude N 39 410, longitude E 116 360 ) on the outskirts of Beijing. The vegetables planted in this field included pakchoi, celery and tomato. Typically, vegetables are grown inside greenhouses (80 m 7 m) that are constructed with clay walls and covered with polyethylene film. One greenhouse was selected for this study, which had a 15year cropping history of continuous vegetable production. Cadmium accumulation in the soil of greenhouse is mainly due to the application of manure and fertilizer with Cd for long time. Soil in the selected greenhouse had the following characteristics: pH (H2O) 7.29, organic matter 2.41%, total Cd 2.55 mg kg1 and DTPAextractable Cd 0.91 mg kg1. The same vegetable species as those used in the pot experiment (Table 1) were grown in the field trial. Conventional fertilization and irrigation practices were adopted in this study. Before planting, 35 kg compound fertilizer, 1000 kg chicken manure and 1000 kg cattle manure were applied to the soil inside the greenhouse. For the convenience of management, the greenhouse area was divided into three parts for growing leafy vegetables, rootstalk vegetables and fruit vegetables. Each vegetable species was grown in four replicate plots that were arranged randomly. The plot sizes were 6, 9 and 12 m2
(17) (8) (8) (12) (12) (17) (17)
for leafy vegetables, rootstalk vegetables and fruit vegetables, respectively. Seeds of leafy vegetables, rootstalk vegetables and cucumber were sown directly onto the seedbeds. For tomato, 4-week-old seedlings were transplanted to the seedbeds. Plant density was determined as follows: 33 104 plants ha1 for leaf vegetables, 4 104 plants ha1 for fruit vegetables, 9 104 and 5 104 plants ha1 for carrot and radish, respectively. The edible parts of the six vegetables were harvested at times appropriate for each species (Table 1). 2.3. Chemical analysis The collected vegetable samples were washed in deionized water, and homogenized in a blender. Fresh sub samples were weighed and digested by HNO3 and HClO4 (4:1). Soil samples were air dried and ground, and digested by HCl/HNO3/HClO4/HF (State Environmental Protection Administration of China, 1997). Total Cd concentrations in soil and vegetable were determined by an atomic absorption spectrophotometer with graphite furnace atomization (GFAAS). Blanks and standard reference materials (Tomato Leaves NIST 1572 and Soil ESS-4 GSBZ50014-88) were included for quality assurance. The recovery ratios were from 89% to 116% throughout the analysis procedures. 2.4. Data analysis The significance of differences between the means of the treatments was evaluated by one-way analysis of variance followed by LSD tests. Linear regression analysis was performed to establish the relationships between the Cd concentrations in the edible parts of vegetables and the Cd concentrations in soil. Statistical analysis were performed with the software SAS (version 8.02). 3. Results and discussion 3.1. Pot experiment In the pot experiment, the growth of all vegetables was not affected by the addition of Cd, because of the relatively low doses of Cd additions. Fig. 1 shows the Cd concentrations in the edible parts of vegetables expressed on a fresh weight basis, because the national allowable limits for Cd are also based on the fresh weight. Cd concentration in vegetables increased linearly with the increasing concentration of Cd added to the soil (Fig. 1). The regression slopes were significantly different (P < 0.01). The slope of the regression lines varied by 28 fold among the six vegetables and followed the order of carrot > pakchoi (Wuyueman) > pakchoi (Xinchun) > Chinese leek > tomato > radish > cucumber (Table 2), indicating large differences in the patterns of Cd accumulation. Some studies have also indicated a linear relationship between the concentration of trace elements in soils and that in crops (Chen, 1991; Ni et al., 2002).
Y. Yang et al. / Journal of Environmental Management 90 (2009) 1117–1122
Cd concentration in the edible parts (mg kg-1 FW)
1.6 Chinese leek
1.6
Xinchun
Wuyueman
1.2
Carrot Radish
1.2
0.8
0.8
0.4
0.4
0.0
1119
0.0 0.0
0.5
1.0
1.5 1.6 1.2
2.0
2.5
0.0
0.5
1.0
1.5
2.0
2.5
Tomato Cucumber
0.8 0.4 0.0 0.0
0.5
1.0
1.5
2.0
2.5
Cd concentration added in soil (mg kg-1) Fig. 1. Cd concentrations in the edible parts of vegetables grown in Cd-spiked soil. Vertical bars represent means SD of three replicates and lines are the fitted linear regression lines.
According to the China environmental quality standard for soils (State Environmental Protection Administration of China, 1995), Cd limits for the soils used for vegetable production are 0.3 and 0.6 mg kg1 for pH < 7.5 and pH > 7.5, respectively. At a Cd level of 0.6 mg kg1, Cd concentrations in six vegetables ranged from 0.02 to 0.43 mg kg1, representing a 21-fold variation. At this level of Cd addition, the national allowable limits of Cd in vegetables (Ministry of Health of the People’s Republic of China and Standardization Administration of China, 2005, Maximum levels of contaminants in foods, 0.2 mg kg1 for pakchoi and leek; 0.1 mg kg1 for carrot and radish; 0.05 mg kg1 for cucumber and tomato) were exceeded in pakchoi (Wuyueman), carrot and tomato. In general, carrot and leafy vegetables accumulate higher Cd concentrations in their edible parts than radish and fruit vegetables. Plants have been shown to vary greatly in metal accumulation from the soil (Cui et al., 2004; Freedman and Hutchinson, 1980; Harrison and Chirgawi, 1989; Kurz et al., 1999; Wang et al., 2006). The results from the present study also showed a large variation among vegetables in Cd concentration, reflecting variation in Cd uptake. In this study, leafy vegetables and carrot had a high risk for Cd accumulation in their edible parts compared with fruit vegetables. Our results are in agreement with previous findings that leafy vegetables and root crops generally have higher Cd concentrations than fruits or seeds (Jinadasa et al., 1997; Lund et al., 1981). Most plant species tend to sequester metals in their roots, with only small amounts of metals being translocated to the above-ground
parts (Kim et al., 1988; Moreno-Caselles et al., 2000). Cataldo et al. (1981) observed that Cd was strongly retained by soybean roots, with only 2% of the accumulated Cd being transported to leaves. Cd accumulation in the vegetables was significantly affected by species. Fruit vegetables appear to be relatively low accumulators of Cd in their edible parts and so would be more suitable species to grow, whereas leafy vegetables tend to accumulate more Cd in leaves. Interestingly, carrot accumulated greater concentration than radish in taproot and appeared to be relatively high accumulator of Cd. Alexander et al. (2006) also identified carrot as intermediate Cd accumulator while French bean and pea were relatively low accumulator and lettuce and spinach were the high accumulator. In addition, two varieties of pakchoi also showed a significant difference in Cd accumulation (P < 0.05). Some similar results had also been found in potato (McLaughlin et al., 1994), lettuce (John and van Laerhoven, 1976), carrot and pea (Alexander et al., 2006). Because linear regression explained a large percentage of the variance (>74%), the regression equation obtained (Table 2) could be used to estimate the threshold of Cd in the tested soil above which the limit for vegetable Cd concentration is breached. The calculated threshold values (Table 2) were below the environmental quality standard for soils (0.6 mg kg1) for pakchoi (Wuyueman), carrot and tomato, suggesting that these vegetable species are at a higher risk of exceeding the national allowable limits. In contrast, the calculated threshold values were higher than
Table 2 Relationship between Cd concentration in the edible parts and that in soil (n ¼ 6), the calculated thresholds of Cd in soil from pot experiment, and bioconcentration factor (BCF) Vegetable species
Regression equation
r2-value
Cd threshold in soil (mg kg1)
BCF in pot experiment
BCF in field trial
Chinese leek Pakchoi (Xinchun) Pakchoi (Wuyueman) Carrot Radish Cucumber Tomato
y ¼ 0.1237x þ 0.0239 y ¼ 0.3063x 0.0233 y ¼ 0.4225x þ 0.003 y ¼ 0.6165x þ 0.0132 y ¼ 0.0357x þ 0.0031 y ¼ 0.0221x þ 0.0031 y ¼ 0.0519x þ 0.0251
0.9419** 0.9750** 0.9655** 0.9954** 0.8997** 0.7365* 0.8629**
1.42 0.73 0.47 0.14 2.71 2.12 0.48
0.15 0.24 0.37 0.62 0.04 0.03 0.09
0.032 0.030 0.039 0.030 0.009 0.004 0.005
**P < 0.01, *P < 0.05.
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Concentration of Cd was generally low in the field study even the treated soil became strongly contaminated with metals (Dudka et al., 1996). Some studies indicated that the aging of Cd in the soil would decrease the bioavailability of heavy metals and reduce the Cd content in the edible part (Gray et al., 1998; Martinez and Motto, 2000). Martinez and Motto (2000) reported that the transformation of heavy metals added as single solutions in mineral soils could become equilibrated after 40 days of incubation. Gray et al. (1998) also found that the proportion of Cd desorbed was decreased by increasing initial contact time. Similarly, Hooda and Alloway (1993) showed that ryegrass accumulated much more Cd when grown on soils spiked with Cd(NO3)2 than on the sewage sludge treated soils. Furthermore, Cd–Zn antagonism should be taken into account for the lower accumulation of Cd in the field experiment. Under ‘‘natural’’ conditions, Cd contamination in most cases is accompanied by Zn contamination. Some researches have proved the enhanced Zn in soils induced reduction in accumulation of Cd (Hart et al., 2002; Podar et al., 2004). However, the order of accumulation of Cd by selected species of vegetables in the pot study was consistent with that in the field study. It is, therefore, possible to select vegetable species that have a lower risk of Cd transfer from contaminated soils. The dose–response equations were derived from plant uptake experiments that were carried out in pot trials amended with soluble cadmium salts. In most cases, the soil metal limits are lower due to the high bioavailability of metals in soil. It is common conception nowadays that the total concentrations of metals in soils are not a good indicator of bioavailability, or a good tool for potential risk assessment, due to the different and complex distribution patterns of metals among various chemical species or solid phases (Brown et al., 1998; Chen et al., 1996; Jackson and Alloway, 1991). Hence the bioavailability of metal to plants should be taken into account as the basis of soil environmental quality criteria and risk assessment. Both Cd uptake and Cd BCF were greater in the pot experiments, also indicating that the Cd accumulation in the edible parts depended on bioavailable Cd amount rather than the total concentration. Relative lower BCF values of vegetables were also found in another field investigation (Wang et al., 2006). The BCF mean values for leek, pakchoi (Xinchun), pakchoi (Wuyueman), carrot, radish, cucumber, tomato in pot experiment were about 4, 7, 9, 20, 3, 6 and 17 times higher than those in the field trial, respectively (Table 2). There were no apparent differences among Chinese leek, pakchoi and carrot in the BCF values. The efficiency of Cd uptake, measured by BCF, varied over a wide range and depended strongly on the vegetable species. The Joint FAO/WHO Expert Committee on Food Additives (WHO, 2001) proposed a provisional tolerable weekly intake (PTWI) of 7 mg Cd kg1 body weight per week for adults, equivalent to 60 mg Cd per day for an average adult weighing 60 kg. Using average vegetable consumption data (Ministry of Agriculture of the People’s Republic of China, 2005; National Bureau of Statistics of China,
the environmental quality standard for soils for Chinese leek, pakchoi (Xinchun), radish and cucumber, indicating that they are at a lower risk. These calculations are based on the assumption that soil Cd has a bioavailability as high as that of the added Cd salt, which is generally not the case (see below) and should be regarded as the worst-case scenario in a risk assessment. The bioconcentration factor (BCF), defined as the ratio of metal concentration in the edible part to the total metal concentration in soil, was used to evaluate the transfer potential of a metal from soil to plant (Alloway et al., 1990; Chumbley and Unwin, 1982; Harrison and Chirgawi, 1989), which is a function of the properties of the metal itself, the soil properties and the genotype of the plant. The BCF values on the basis of fresh weight varied among vegetables, indicating the difference in the accumulation ability of Cd for six vegetables (Table 2). Carrot had the highest BCF value (0.62), which was about 20 times higher than that of cucumber in the pot experiment. To explain whether differences in the Cd concentration could be due to different water contents of the vegetables, Cd concentrations are also expressed on a dry weight basis (Table 3). Higher Cd concentrations on the dry weight basis were also observed in carrot and leafy vegetables. However, the highest Cd concentration on the dry weight basis was found in pakchoi (Wuyueman), whereas carrot had the highest Cd concentration on the fresh weight basis. A similar ranking in Cd concentration for the fresh weight basis and dry weight basis was found for other vegetables. 3.2. Field trial In the field trial, the Cd concentrations in the edible parts of the six vegetables ranged from 0.01 to 0.1 mg kg1, which were below the national allowable limits (Fig. 2), even though the soil had a substantially elevated concentration of Cd (2.55 mg kg1). Higher Cd concentrations were found in Chinese leek, pakchoi (Xinchun and Wuyueman) and carrot than in radish, cucumber and tomato. Despite the much lower concentrations recorded in the field trial than in the pot experiment, the ranking of the six vegetables in terms of Cd accumulation was similar in the two experiments, indicating that species performed consistently under different growth conditions. Furthermore, the vegetable species showed a similar ranking in Cd concentration based on the fresh weight and on the dry weight (Fig. 2). The Cd concentrations in the edible parts of vegetables grown in Cd-spiked soil in the pot experiment and in the field Cd-contaminated soil showed large differences. The Cd concentrations were above the allowable limits for leafy vegetables and carrot grown in 2.0 mg kg1 Cd-spiked soil, but were below the limit in the field experiment with a soil Cd of 2.55 mg kg1. It is clear that the bioavailability of Cd in the soil in the field trial was much lower than that of the freshly spiked Cd in the pot experiment. Bioavailability of Cd in a field contaminated soil was about 4–18% of that of the freshly added Cd in the pot experiment.
Table 3 Cd concentrations in the edible parts of vegetables grown in Cd-amended soil (mg kg1 dry weight) Vegetable species
Chinese leek Pakchoi (Xinchun) Pakchoi (Wuyueman) Carrot Radish Cucumber Tomato
Added soil Cd (mg kg1) 0.0
0.3
0.6
1.0
1.5
2.0
0.05 0.01 0.10 0.05 0.38 0.12 0.15 0.27 0.01 0.02 0.08 0.08 0.05 0.01
0.48 0.08 0.63 0.42 2.07 1.15 1.61 0.14 0.19 0.05 0.05 0.02 0.63 0.17
1.06 0.17 1.79 0.70 4.63 1.24 2.51 0.61 0.48 0.25 0.24 0.06 0.87 0.15
1.48 0.18 3.33 0.56 5.02 1.30 3.81 0.42 0.82 0.49 0.44 0.02 0.94 0.06
1.63 0.23 4.30 0.88 5.81 0.13 6.00 2.14 0.66 0.30 0.78 0.10 1.26 0.06
1.88 0.07 6.53 1.58 10.87 0.94 7.02 1.16 1.00 0.15 0.55 0.16 1.48 0.35
Values are presented as mean SD of three replicates.
Y. Yang et al. / Journal of Environmental Management 90 (2009) 1117–1122
a
0.15
0.09 0.06 0.03
at o To
m
be uc um
ad R
r
is h
t ro ar C
C
hi
ne
Xi n
se
le
ch un W uy ue m an
ek
0
C
b
2.0 1.6 1.2 0.8 0.4
o at m To
um uc C
R
ad
is
be
r
h
t ro ar
m ue uy W
C
n hu Xi
nc
le se C
hi
ne
an
0.0 ek
Cd concentration in the edible parts (mg kg-1)
0.12
Fig. 2. Cd concentrations in the edible parts of vegetables grown in Cd-contaminated soil on the fresh weight (a) and dry weight (b). Vertical bars represent means SD of four replicates.
2005) and the Cd concentrations in the field trial, the average Cd intake from consumption of the six vegetables was estimated to be 10 mg day1 per person, which accounts for 16.7% of the PTWI. This is likely to represent the worst case scenario, because only a relatively small proportion of vegetable farmland in Beijing is contaminated with Cd. 4. Conclusions The present study showed a large variation among the six major vegetable species in the accumulation of Cd. We obtained the same results from the pot experiment and the field trial. Furthermore, the bioavailability of Cd was much lower in the field contaminated soil than in the artificially contaminated soil used in the pot experiment. The study provided data on the Cd accumulation of six major vegetable species. The results showed that selection of vegetables with low Cd uptake on contaminated soil could contribute to reducing Cd transfer from soil to food crops, and subsequently human Cd intake. Acknowledgments The authors are grateful to the financial support from the key project of Ministry of Agriculture, China (Project number: 2003Z53), and from the vegetable technological project of Beijing Agricultural Bureau. H.-F L. was supported by China Scholarship Council for a study visit to Rothamsted Research. We thank Dr. Fangjie Zhao for his helpful comments and polishing of the English in the manuscript during the study in Rothamsted Research. References Ahumada, I., Mendoza, J., Navarrete, E., Ascar, L., 1999. Sequential extraction of heavy metals in soils irrigated with wastewater. Communications in Soil Science and Plant Analysis 30, 1507–1519. Alexander, P.D., Alloway, B.J., Dourado, A.M., 2006. Genotypic variations in the accumulation of Cd, Cu, Pb and Zn exhibited by six commonly grown vegetables. Environmental Pollution 144, 736–745.
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