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Environmental Pollution xx (2005) 1e7
Cadmium contamination in orchard soils and fruit trees and its potential health risk in Guangzhou, China
J.T. Li a, J.W. Qiu b, X.W. Wang a, Y. Zhong a, C.Y. Lan a,*, W.S. Shu a,*
a School of Life Sciences and State Key Laboratory of Biocontrol, Sun Yat-sen (Zhongshan) University, Guangzhou 510275, PR China b Department of Biology, Hong Kong Baptist University, Kowloon, Hong Kong, PR China Received 6 August 2005; received in revised form 19 September 2005; accepted 14 October 2005
Carambola fruit can accumulate high levels of cadmium and may be a health risk for humans.
Abstract
This study examines cadmium (Cd) contamination in orchard soils and fruit trees in Guangzhou, China, and assesses its potential health risk. Soils and tissues samples of three species of fruit trees were collected from three orchards. The average soil Cd concentration was 1.27, 1.84 and 0.68 mg/kg in orchards I, II, and III, respectively. The carambola (Averrhoa carambola) accumulated exceptionally high concentrations of Cd (7.57, 10.84, 9.01 and 2.15 mg/kg dw in root, twig, leaf and fruit, respectively), being 6.0e24 times and 4.0e10 times the corresponding tissue Cd in the longan (Dimocarpus longan) and wampee (Clausena lansium), respectively. Furthermore, all Cd concentrations (0.04e0.25 mg Cd/kg fw) of the fruits exceeded the tolerance limit of cadmium in foods of PR China (0.03 mg/kg fw). Our results indicate that the carambola tree has high Cd accumulation capacity and might be a Cd accumulator; and its fruit, among the three species of fruits studied, also poses the highest potential health risk to local residents. Ó 2005 Elsevier Ltd. All rights reserved.
Keywords: Cadmium; Accumulator; Fruits; Health risk
1. Introduction have resulted in the release of significant quantities of Cd to the environment (WHO, 1992; Manta et al., 2002; Komarnicki, Cadmium (Cd) contamination of agricultural soil is of 2005). Cadmium in soil is easily accumulated by plants worldwide concern due to the food safety issues and poten- through the root system, compared with other toxic metals tial health risks (Dudka et al., 1996; McLaughlin et al., 1999; (Thuvander and Oskarsson, 1998). Hence, the soil-plant- Dorris et al., 2002; Tsadilas et al., 2005). Cadmium can accu- human transfer of Cd has been considered as a major pathway mulate gradually in the human body, where it may lead to of human exposure to soil Cd (Cui et al., 2004). a number of adverse health effects, such as nephrotoxicity Environmental pollution of Cd occurs widely in China re- and osteotoxicity (WHO, 1992). sulting from its rapidly economic development during the The two major sources of Cd in soils are natural occurrence past two decades (Jin et al., 2004). The potential health risks derived from parent materials and anthropic activities (WHO, due to soil Cd contamination have been well assessed in 1992). Numerous human activities, such as mining, waste dis- China. However, most of the previous investigations have posal, vehicle exhausts and phosphate fertilizer application, focused on rice (Wang et al., 2001; Xiong et al., 2004), wheat (Nan and Cheng, 2001; Nan et al., 2002) and vegetables (Zhou et al., 2000; Cui et al., 2004). Very little information is available on Cd accumulation in orchard soils and fruits * Corresponding authors. Tel.: þ86 20 84036296; fax: þ86 20 84113652. (Santos et al., 2004). In Guangzhou, a major city in southern E-mail addresses: [email protected] (C.Y. Lan), [email protected] (W.S. Shu). China, no such information is available for the assessment of
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health risk. Therefore, the objectives of this work were to: (1) The aerial parts were sampled by using a pair of stainless steel scissors, and quantify the Cd contamination in orchard soils and fruits; (2) the roots (about 0.5e1 cm in diameter) were scooped up using a stainless evaluate the potential health risk of human fruits consumption; shovel. All samples were stored in polyethylene bags in the field and trans- ferred to the laboratory within 3 h for preparation. and (3) relate Cd accumulation in fruits and the associated soil After removal of visible pieces of plant residues, the soils were air-dried, conditions. crushed, sieved through a 2-mm screen, then pulverized and passed through a 0.2-mm mesh sieve. The plant samples were washed with tap water followed 2. Materials and methods by deionized water to remove soil particles or dust adhering to the plant sur- face and dried with tissue paper. The fruits were separated into edible and in- 2.1. Site description edible parts. All of the plant samples were then oven-dried at 70 C for 72 h to a constant weight. Fresh and dry edible fruits parts were weighed. Prior to The present investigation was conducted in Guangzhou City (22 26# to chemical analysis, all dry plant samples were ground into fine powder by 23 56#N, 112 57# to 114 03#E), the capital of Guangdong Province, southern a stainless steel mill. China. The area has a typical subtropical monsoonal climate, with annual av- erage temperature of 23.0 C and rainfall of 1782.9 mm (Guangzhou Year- 2.3. Chemical analysis book, 2003), which is very suitable for the growth of most subtropical fruits. The carambola (Averrhoa carambola), the longan (Dimocarpus longan) Soil pH value was measured in a 1:2.5 (w/v) ratio of soil to distilled water and the wampee (Clausena lansium) studied in this work are three species of using a pH meter. Soil organic matter (OM) content was determined by a wet- the most favorite and economically important fruits of the city, and they are combustion method (ISSCAS, 1978). Soil cation exchange capacity (CEC) also very popular in many southeast Asian countries. In 2002, the production was determined by the BaCl2 compulsive exchange method (Gillman and of the carambola and longan in Guangzhou amounted to 6875 and 37,968 tons, Sumpter, 1986). For total Cd determination, the soil samples were digested respectively (Guangzhou Yearbook, 2003). Three large orchards with different in 4 ml of ‘‘aqua-regia’’ (HNO3/HCl ¼ 1/3, v/v; McGrath and Cunliffe, irrigation water sources were included in this study (Fig. 1). Orchard I and or- 1985). The ‘‘plant available’’ Cd in soils was extracted with a diethylenetet- chard II are located in the same district (Hai-Zhu District), and have direct ac- raminepentaacetic acid (DTPA) solution (0.005 M DTPA þ 0.005 M cess to the Pearl River through irrigation channels. Orchard I is about 3 km and CaCl2 þ 0.1 M TEA, pH ¼ 7.3; Lindsay and Norvell, 1978). Total Cd in plant orchard II about 1 km from the town center, whereas orchard III is located in materials was extracted with a mixture of concentrated HNO3 and concentrated another district (Tian-He District), being inaccessible to the Pearl River. HClO4, at 5:1 (v/v) (Allen, 1989). Cd concentrations were determined using an atomic absorption spectrophotometer (Hitachi-Z-5300). Quality control of soil and plant materials analysis was performed using a certified concentration of 2.2. Sampling and preparation Cd solution (GBW-08612) obtained from the National Center for Standard Materials. The sampling was carried out in August 2004. Ten samples of soils and plant tissues (including root, twig, leaf and fruit) of the carambola were col- 2.4. Data analysis lected from each of the three orchards (Fig. 1). The roots of the carambola were collected only in orchard I, because the sampling of roots was not per- 2.4.1. Soil Cd contamination assessment mitted in the other orchards. Each soil sample (about 1 kg) was a composite The degree of Cd contamination in the orchard soils was determined by the of five sub-samples taken from a depth of 0e20 cm. The carambola samples geo-accumulation index (I-geo) as proposed by Muller (1969): were collected from the associated soil-sampling sites for correlation purpose. The carambola trees in the three orchards belonged to the same local cultivar I-geo ¼ log2ðCn=1:5BnÞ (Averrhoa carambola cv. Hua-Di). In orchard I, since the longan (Dimocarpus
longan cv. Shi-Jia) and wampee (Clausena lansium cv. Ji-Xin) trees were where Cn represents total Cd concentration in orchard soil, Bn is the natural planted along with the carambola within 5 m 5 m plots, so 10 tissue (root, background soil Cd concentration in Guangzhou (0.14 mg/kg; GDPEMC, twig, leaf and fruit) samples of the two trees were also collected, respectively. 1990) and 1.5 is a correction factor. Based on I-geo, the Cd contamination
Fig. 1. Map of Guangzhou, showing the location of orchards I, II and III. Soil and tissues of tree samples were collected from the three orchards as indicated by filled triangles, and the sampling sites in the orchards are indicated by filled circles. The main tributes of the Pearl River and the irrigation channels connecting with them are shown as filled curves. The empty curves represent the roads. ARTICLE IN PRESS
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levels of soil are classified into seven grades: 0 (grade 0) represents uncontam- potentially ecological risk (Liu et al., 2002). Both orchards I inated; 0-1 (grade 1), slightly moderately contaminated; 1-2 (grade 2), moder- and II were irrigated with the Pearl River water, whereas or- ately contaminated; 2-3 (grade 3), moderately severely contaminated; 3-4 chard III was irrigated with tap water. In addition to irrigation (grade 4), severely contaminated; 4-5 (grade 5), severely extremely contami- nated; 5-6 (grade 6), extremely contaminated (Muller, 1969). water, the sludge of the irrigation channels, which came essen- tially from the surface sediment of the Pearl River, was used as nutrient amendment in orchards I and II. A lot of small indus- 2.4.2. Cd transfer coefficient (Tc) The Cd transfer coefficient (Tc) reflects the transfer efficiency of Cd from tries such as textile firms, circuit board manufacturers, toy soil to plant. It is an important parameter in the evaluation of the potential makers and leather tanneries in this district might also contrib- health risk of human exposure to soil Cd (US EPA, 1992). The Tc of Cd ute to the overall pollution of the river. The industrial effluent, from soils to fruit (edible part) is calculated as Cd concentration in fruit (on often not properly treated, has been known to adversely affect fresh weight basis) divided by total Cd concentration in soil where the fruit tree is planted (US EPA, 1992). the environment (Tao and Hills, 1999). The significantly higher Cd concentration in orchard II than that in orchard I was possibly attributed to its shorter distance from the town 2.4.3. Statistical analysis All statistical analyses were performed using the statistical package SPSS where most of the factories were located. The average Cd con- 10.0 for Windows (SPSS Inc., USA). Correlation between Cd concentrations centration (0.68 mg/kg) in the soil of orchard III, being the in the soils and in the plant tissues was performed using the Pearson correla- lowest in this study, was similar to that of Hangzhou tion procedure. Difference in Cd concentrations among plant tissues and soil (0.80 mg/kg; Zhang and Ke, 2004), but was much higher samples collected from different orchards was detected using one-way ANOVA, followed by multiple comparisons using the least significant differ- than that of Shanghai (0.35 mg/kg; Hu et al., 2004). In Hong ence (LSD) test. The level of significance was set at P < 0.05 (two-tailed). Kong, another major city in the Pearl River Delta, the mean Cd concentration in urban and orchard soil was 2.2 mg/kg (Li et al., 2001) and 1.4 mg/kg (Chen et al., 1997), respectively. 3. Results and discussion These data indicate that high Cd concentration in soils might be a common environmental phenomenon in both major cities 3.1. Cadmium contamination in soil of the Pearl River Delta. Since soil Cd contamination may dramatically limit land Total concentrations of Cd in soil samples are presented in use, critical soil Cd concentration has been proposed in various Table 1. The average concentration of Cd was 1.27, 1.84 and countries. In China, the Environment Quality Standard for Soil 0.68 mg/kg in orchards I, II and III, respectively. The soil Cd Cd level in farmland, horticulture land, tea plantation soil, or- concentration in orchards I and II was approximately 1.9 and chards and grazing land stipulated the maximum concentra- 2.7 times that in orchard III. The mean I-geo value (Table 1) tions of 0.3 mg/kg at soil pH < 6.5 and 0.6 mg/kg at soil pH was 2.52, 3.02 and 1.64 in orchards I, II, and III, respectively, between 6.5 and 7.5 (SEPAC, 1995). It was clear that Cd con- suggesting that all three orchards were contaminated by Cd at centrations in the soils from all of the three orchards exceeded different levels: moderate-severe (grade 3, orchard I), severe the national soil standard. Therefore, the soils are not suitable (grade 4, orchard II) and moderate (grade 2, orchard III). for cultivation without remediation. These results were probably due to the fact that these orchards used different irrigation water. 3.2. Cadmium accumulation in fruit trees and its Rapid urbanization and industrialization has taken place in potential health risk the areas surrounding the lower reaches of the Pearl River (the Pearl River Delta), including Guangzhou, since early 1980s. Fig. 2 shows Cd concentrations in tissues of the three dif- This rapid development has resulted in severe pollution of ferent species of fruit trees planted in orchard I. In the same the Pearl River (Liu et al., 2003; Chen et al., 2004; Ip et al., tissue, Cd concentration in different species varied greatly. 2004). Heavy metal levels in the surface sediment of the es- The highest Cd concentrations were observed in the carambo- tuary have generally increased over the last two decades la, and the lowest Cd concentrations generally occurred in the (Li et al., 2000). The maximum Cd concentration in the sur- longan. The exceptionally high Cd concentrations in the root, face sediment reached 1.1 mg/kg and showed the highest twig, leaf and fruit (edible part) of the carambola (7.57, 10.84, 9.01 and 2.15 mg/kg dw, respectively) were 6.0, 24, 22 and 6.5 Table 1 times of those of the longan, respectively. The foliar concen- Selected properties of the orchard soils (mean SD, n ¼ 10) trations of Cd in both wampee and longan were within the nor- Orchard _ Orchard II Orchard III mal range (0.1e2.4 mg/kg) of uncontaminated woody plants pH 4.93 0.54 a* 5.16 0.31 a 4.11 0.13 b (Alloway, 1995). However, carambola foliar Cd (9.01 mg/kg) OM content (g/kg) 19.69 13.28 b 12.35 5.36 b 30.36 9.04 a exceeded the normal range greatly. Moreover, among the CEC (cmol/kg) 25.41 9.77 b 22.11 10.65 b 36.98 5.48 a three species studied, the carambola seemed to be the only Total Cd (mg/kg) 1.27 0.45 b 1.84 0.73 a 0.68 0.14 c DTPA-Cd (mg/kg) 0.66 0.41 a 0.72 0.33 a 0.05 0.02 b species showing bio-accumulation of Cd, with tissue Cd levels (DTPA-Cd)% 48.43 22.86 a 39.71 13.77 a 7.57 1.32 b greatly exceeding Cd levels in the associated soils. The bio- I-geo 2.52 0.44 b 3.02 0.48 a 1.64 0.28 c accumulation coefficient (7.0) was much higher than that *Numbers followed by different letters in the same row indicate a significant found in Salix viminalis (0.83), a species known for its Cd difference (P < 0.05). accumulation capacity (Rosselli et al., 2003). Uptake and ARTICLE IN PRESS
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A B Carambola Wampee a Longan 16 a 0.30 0.30 14 a 0.25 0.25 12 a a 0.20 10 0.20
8 0.15 0.15 Tc of Cd 6 0.10 b 0.10 4 b b b a b 0.05 b 0.05
Cd mg/kg (on dry weight basis) b b 2 Cd mg/kg (on fresh weight basis) b b b b 0 0.00 0.00 Root Twig Leaf Fruit Cd in fruit Tc of fruit
Fig. 2. Cadmium concentrations (mean þ SD, n ¼ 10) in the tissues of different fruit trees in orchard I and Cd transfer coefficient (Tc) of the three species of fruits (edible part). The error bars represent standard deviation (SD). Lower case letters indicate multiple comparisons among different fruit trees, bars with different letters are significantly different (P < 0.05). accumulation of heavy metals in plants may follow two differ- (on dry weight basis) respectively. These results further ent pathways, i.e., the root system and the foliar surface. demonstrated that the carambola tree had a special ability to Because Cd was below the detection limit (0.1 mg/L) in sus- accumulate Cd from soil and could be a Cd accumulator. pended particles in air samples collected from Guangzhou In China, the tolerance limit of cadmium in foods is (Teng et al., 1999), and the plant samples were washed with 0.03 mg/kg (MHPRC, 1994). Cadmium in all three species tap and deionized water before digestion, it was unlikely of fruits (edible part) exceeded the tolerance limit more or that the high Cd concentrations in the carambola samples less (Fig. 2). The carambola fruits from orchard I contained were the result of air-borne contamination. The high foliar the highest Cd level (0.25 mg/kg, on a fresh weight basis), Cd reflected a special ability of the carambola to accumulate which was 8.4 times the tolerance limit. Cadmium concen- Cd from soil. Therefore, the carambola might be considered trations in the carambola fruits obtained from orchard II as a Cd accumulator. (0.19 mg/kg) and orchard III (0.11 mg/kg), despite being lower In general, Cd accumulators can transfer a large proportion than those in orchard I, were still much higher than the toler- of the pollutant from their roots to the above-ground tissues ance limit. These gave the carambola fruits a high average Tc (Rosselli et al., 2003). In this work, the order of Cd accumu- (0.16), being much higher than those of the other two species lation in the carambola tissues (twig > leaf > root > fruit) (Fig. 2). The Tc of carambola fruits (edible part) was relatively was similar to that of the wampee (twig > root > leaf > fruit). high, and close to those of the vegetables with high Tc (Cui Large proportions (74% in the carambola and 64% in the et al., 2004), such as Apium graveolens L. (0.16) and Zingiber wampee) of total accumulated Cd in the plants were located officinale Rosc. (0.15). Such high Tc values indicate high in its above-ground tissues. The result was similar to the find- potential health risks (US EPA, 1992). Therefore, among the ings of Robinson et al. (2000) who reported that most Cd three species of fruits, the carambola posed the highest poten- (about 55%) accumulated by the poplar tree (Beaupre´) sam- tial health risk to local residents. According to the provisional pled from a contaminated site in northern France was in the tolerable weekly intake (PTWI) Cd values suggested by WHO above-ground tissues (twigs and leaves). However, in the lon- (1989) (0.04 mg/day for a 40 kg child), a 40 kg child should gan, only about 45% of the total Cd accumulated was in the not eat more than 0.16, 0.66, or 1.0 kg (on fresh weight basis) above-ground tissues. The pattern of Cd distribution in the lon- of the carambola, wampee or longan fruits from orchard I per gan (root > twig > leaf > fruit) was typical of non-Cd accu- day. During the harvesting season, the local residents on mulators, such as Mougeot Rowan (Rosselli et al., 2003) and Scotch pine (Kim et al., 2003). Table 2 Table 2 shows Cd concentrations in tissues of the carambola Cadmium concentration (mean SD, n ¼ 10) in the carambola trees of the three orchards and Cd transfer coefficient (T ) (edible part) collected from different orchards. In the same tissue, Cd c _ concentrations varied greatly among the orchards. Except for Orchard Orchard II Orchard III the root, carambola tissues collected from orchards I and or- Root (mg/kg, dw) 7.57 2.96 ee chard II contained significantly higher Cd levels than those Twig (mg/kg, dw) 10.84 4.21 a* 10.97 5.27 a 5.23 1.04 b Leaf (mg/kg, dw) 9.01 2.98 a 8.54 4.26 a 4.03 1.41 b from orchard III. However, high Cd bio-accumulation coeffi- Fruit(edible part) (mg/kg, dw) 2.15 0.51 a 1.64 0.44 b 0.92 0.25 c cients were found in all three orchards (7.0 in orchard I, 4.6 Fruit (edible part) (mg/kg, fw) 0.25 0.06 a 0.19 0.05 b 0.11 0.03 c in orchard II, and 5.8 in orchard III). The average Cd concen- Tc (edible part) 0.21 0.06 a 0.11 0.05 b 0.16 0.03 b trations in twigs, leaves and fruits (edible part) of carambola *Numbers followed by different letters in the same row indicate a significant trees from different orchards were 9.01, 7.16 and 1.56 mg/kg difference (P < 0.05). e, data was unavailable. ARTICLE IN PRESS
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Table 3 Correlation matrix of soil properties, Cd in soil and Cd in tissues of carambola trees Total Cd DTPA-Cd (DTPA-Cd)% pH OM content CEC Cd in twig Cd in leaf DTPA-Cd 0.82* (DTPA-Cd)% 0.46* 0.85* pH 0.72* 0.84* 0.80* OM content 0.65* 0.78* 0.69* 0.71* CEC 0.28 0.47* 0.57* 0.46* 0.45* Cd in twig 0.75* 0.64* 0.41* 0.50* 0.55* 0.32 Cd in leaf 0.75* 0.62* 0.41* 0.53* 0.50* 0.35 0.96* Cd in fruit 0.52* 0.64* 0.65* 0.52* 0.46* 0.36* 0.72* 0.76* *Correlation is significant at the 0.05 probability level (two-tailed).
average consume about 0.5 kg of carambola per day per 2004). The effect of organic matter on DTPA-Cd could prob- person; hence, great attention should be paid to the potential ably be explained by its ability to form chelate complexes with health risk to them. Cd and its high CEC (Karaca, 2004). In this work, a signifi- cantly negative correlation (r ¼ 0.47) was found between DTPA-Cd and soil CEC. This observation was consistent 3.3. Relationships between soil properties, with the fact that high soil CEC decreased the bioavailability soil Cd and carambola tissues Cd of Cd (Miner et al., 1997). Indeed, a similar observation was also reported by Adhikari and Singh (2003). The plant uptake of heavy metal from soil is influenced by soil properties, such as pH and organic matter (McLaughlin 4. Conclusions et al., 1999; Evangelou et al., 2004). Results of Pearson corre- lation analysis among soil properties, soil Cd and carambola 1. Cadmium concentrations in the orchard soils studied ex- tissues Cd are shown in Table 3. Cadmium concentration in ceeded the Chinese National Environment Quality Standard the carambola tissues was positively correlated (P < 0.05) for Soil. The contamination level of the three orchards with its total and DTPA-extractable concentration in the soil, ranked moderate-severe (grade 3, in orchard I), severe and with the percentage of DTPA-Cd and soil pH value, while (grade 4, in orchard II) or moderate (grade 2, in orchard III). was negatively correlated (P < 0.05) with soil organic matter 2. The three fruit trees studied differed significantly in tissue content. Cadmium concentration in the tissues of the other Cd levels. For the same tissue, the lowest Cd concentra- two plants was also positively correlated (P < 0.05) with its tions generally occurred in the longan, while the highest total and DTPA-extractable concentrations in the soils (data Cd concentrations were found in the carambola. The car- not shown). Total soil heavy metal concentration is commonly ambola collected from three orchards all showed high used to indicate the degree of contamination (Karaca, 2004), bio-accumulation coefficients, indicating its potential as although DTPA-extractable concentration provides a more a Cd accumulator. suitable chemical evaluation of the amount of metals available 3. Cadmium concentrations in all three species of fruits for plant uptake (Lindsay and Norvell, 1978; Pretuzzelli, 1989; (edible parts) sampled were above the national guidance Zufiaurre et al., 1998). However, our results showed that both for food. Among the three species, the carambola fruits parameters could be used to estimate Cd concentrations in car- had high average T (0.16), and posed the highest potential ambola tissues. The correlation between Cd in carambola tis- c health risk to local residents. sues (except fruits) and the DTPA-extractable Cd was slightly 4. Cadmium in the carambola tissues was significantly corre- inferior to that between Cd in carambola tissues and total soil lated with its total and DTPA-extractable concentrations in Cd (Table 3). This was probably because of the significantly soils. DTPA-Cd was also significantly correlated with soil lower concentrations of DTPA-Cd in orchard III (Table 1). pH value and soil organic matter content, indicating that The high percentages of DTPA-Cd, especially in the soils soil pH value and soil organic matter content are key fac- of orchards I and II, were likely due to the low soil pH values tors governing Cd uptake of the carambola from soil. (Table 1), which might be caused by the frequent acid rain in Guangzhou (Xu et al., 2001). However, a significantly positive correlation (r ¼ 0.84) was found between DTPA-Cd and soil Acknowledgements pH. The result was inconsistent with results of previous studies (Arnesen and Singh, 1998; Cieslinski et al., 1998; Nigam et al., The authors would like to acknowledge financial support 2001; Zhou et al., 2003). This inconsistency might be partly from the National ‘‘863’’ Project of China (No. due to the relatively narrow soil pH range (4.1 pH 5.2) 2003AA645010-3), the National Science Foundation of China in this work, and further investigation is needed. (No. 40471117), the Key Project of Science and Technology DTPA-Cd was negatively correlated with soil organic mat- of Ministry of Education of China (No. 031280) and the ter content (r ¼ 0.78). The result agreed well with those Key Project of Guangzhou Municipal Science & Technology found in the literature (Arnesen and Singh, 1998; Karaca, Commission (No. 200251-C7061). ARTICLE IN PRESS
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