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Cadmium contamination in orchard soils and fruit trees and its potential health risk in Guangzhou, China
a,
J.T. Li a, J.W. Qiu b, X.W. Wang a, Y. Zhong a, C.Y. Lan a, , W.S. Shu
- *
- *
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,
2005). Cadmium in soil is easily accumulated by plants through the root system, compared with other toxic metals
(Thuvander and Oskarsson, 1998). Hence, the soil-plant-
human transfer of Cd has been considered as a major pathway of human exposure to soil Cd (Cui et al., 2004).
Environmental pollution of Cd occurs widely in China resulting from its rapidly economic development during the past two decades (Jin et al., 2004). The potential health risks due to soil Cd contamination have been well assessed in China. However, most of the previous investigations have
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 (Santos et al., 2004). In Guangzhou, a major city in southern China, no such information is available for the assessment of
Cadmium (Cd) contamination of agricultural soil is of worldwide concern due to the food safety issues and poten-
tial health risks (Dudka et al., 1996; McLaughlin et al., 1999; Dorris et al., 2002; Tsadilas et al., 2005). Cadmium can accu-
mulate gradually in the human body, where it may lead to a number of adverse health effects, such as nephrotoxicity and osteotoxicity (WHO, 1992).
The two major sources of Cd in soils are natural occurrence derived from parent materials and anthropic activities (WHO, 1992). Numerous human activities, such as mining, waste disposal, vehicle exhausts and phosphate fertilizer application,
* Corresponding authors. Tel.: þ86 20 84036296; fax: þ86 20 84113652.
E-mail addresses: [email protected] (C.Y. Lan), [email protected] (W.S. Shu).
0269-7491/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2005.10.016
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The aerial parts were sampled by using a pair of stainless steel scissors, and the roots (about 0.5e1 cm in diameter) were scooped up using a stainless shovel. All samples were stored in polyethylene bags in the field and transferred to the laboratory within 3 h for preparation.
health risk. Therefore, the objectives of this work were to: (1) quantify the Cd contamination in orchard soils and fruits; (2) evaluate the potential health risk of human fruits consumption; and (3) relate Cd accumulation in fruits and the associated soil conditions.
After removal of visible pieces of plant residues, the soils were air-dried, 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 by deionized water to remove soil particles or dust adhering to the plant surface and dried with tissue paper. The fruits were separated into edible and inedible 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 chemical analysis, all dry plant samples were ground into fine powder by a stainless steel mill.
2. Materials and methods
2.1. Site description
The present investigation was conducted in Guangzhou City (22ꢀ26# to
23ꢀ56#N, 112ꢀ57# to 114ꢀ03#E), the capital of Guangdong Province, southern China. The area has a typical subtropical monsoonal climate, with annual average temperature of 23.0 ꢀC and rainfall of 1782.9 mm (Guangzhou Yearbook, 2003), which is very suitable for the growth of most subtropical fruits. The carambola (Averrhoa carambola), the longan (Dimocarpus longan) and the wampee (Clausena lansium) studied in this work are three species of the most favorite and economically important fruits of the city, and they are also very popular in many southeast Asian countries. In 2002, the production of the carambola and longan in Guangzhou amounted to 6875 and 37,968 tons, respectively (Guangzhou Yearbook, 2003). Three large orchards with different irrigation water sources were included in this study (Fig. 1). Orchard I and orchard II are located in the same district (Hai-Zhu District), and have direct access to the Pearl River through irrigation channels. Orchard I is about 3 km and orchard II about 1 km from the town center, whereas orchard III is located in another district (Tian-He District), being inaccessible to the Pearl River.
2.3. Chemical analysis
Soil pH value was measured in a 1:2.5 (w/v) ratio of soil to distilled water using a pH meter. Soil organic matter (OM) content was determined by a wetcombustion method (ISSCAS, 1978). Soil cation exchange capacity (CEC) was determined by the BaCl2 compulsive exchange method (Gillman and Sumpter, 1986). For total Cd determination, the soil samples were digested in 4 ml of ‘‘aqua-regia’’ (HNO3/HCl ¼ 1/3, v/v; McGrath and Cunliffe, 1985). The ‘‘plant available’’ Cd in soils was extracted with a diethylenetet-
- raminepentaacetic acid (DTPA) solution (0.005
- M
- DTPA þ 0.005
- M
CaCl2 þ 0.1 M TEA, pH ¼ 7.3; Lindsay and Norvell, 1978). Total Cd in plant materials was extracted with a mixture of concentrated HNO3 and concentrated 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 Cd solution (GBW-08612) obtained from the National Center for Standard Materials.
2.2. Sampling and preparation
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 collected 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 permitted in the other orchards. Each soil sample (about 1 kg) was a composite of five sub-samples taken from a depth of 0e20 cm. The carambola samples were collected from the associated soil-sampling sites for correlation purpose. The carambola trees in the three orchards belonged to the same local cultivar (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 planted along with the carambola within 5 m  5 m plots, so 10 tissue (root, twig, leaf and fruit) samples of the two trees were also collected, respectively.
2.4. Data analysis
2.4.1. Soil Cd contamination assessment
The degree of Cd contamination in the orchard soils was determined by the geo-accumulation index (I-geo) as proposed by Muller (1969):
I-geo ¼ log2ðCn=1:5BnÞ where Cn represents total Cd concentration in orchard soil, Bn is the natural background soil Cd concentration in Guangzhou (0.14 mg/kg; GDPEMC, 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.
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levels of soil are classified into seven grades: 0 (grade 0) represents uncontaminated; 0-1 (grade 1), slightly moderately contaminated; 1-2 (grade 2), moderately contaminated; 2-3 (grade 3), moderately severely contaminated; 3-4 (grade 4), severely contaminated; 4-5 (grade 5), severely extremely contaminated; 5-6 (grade 6), extremely contaminated (Muller, 1969).
potentially ecological risk (Liu et al., 2002). Both orchards I and II were irrigated with the Pearl River water, whereas orchard III was irrigated with tap water. In addition to irrigation water, the sludge of the irrigation channels, which came essentially from the surface sediment of the Pearl River, was used as nutrient amendment in orchards I and II. A lot of small industries such as textile firms, circuit board manufacturers, toy makers and leather tanneries in this district might also contribute to the overall pollution of the river. The industrial effluent, often not properly treated, has been known to adversely affect 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 where most of the factories were located. The average Cd concentration (0.68 mg/kg) in the soil of orchard III, being the lowest in this study, was similar to that of Hangzhou (0.80 mg/kg; Zhang and Ke, 2004), but was much higher than that of Shanghai (0.35 mg/kg; Hu et al., 2004). In Hong 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. These data indicate that high Cd concentration in soils might be a common environmental phenomenon in both major cities of the Pearl River Delta.
2.4.2. Cd transfer coefficient (Tc)
The Cd transfer coefficient (Tc) reflects the transfer efficiency of Cd from soil to plant. It is an important parameter in the evaluation of the potential health risk of human exposure to soil Cd (US EPA, 1992). The Tc of Cd from soils to fruit (edible part) is calculated as Cd concentration in fruit (on fresh weight basis) divided by total Cd concentration in soil where the fruit tree is planted (US EPA, 1992).
2.4.3. Statistical analysis
All statistical analyses were performed using the statistical package SPSS
10.0 for Windows (SPSS Inc., USA). Correlation between Cd concentrations in the soils and in the plant tissues was performed using the Pearson correlation procedure. Difference in Cd concentrations among plant tissues and soil samples collected from different orchards was detected using one-way ANOVA, followed by multiple comparisons using the least significant difference (LSD) test. The level of significance was set at P < 0.05 (two-tailed).
3. Results and discussion
3.1. Cadmium contamination in soil
Since soil Cd contamination may dramatically limit land use, critical soil Cd concentration has been proposed in various countries. In China, the Environment Quality Standard for Soil Cd level in farmland, horticulture land, tea plantation soil, orchards and grazing land stipulated the maximum concentrations of 0.3 mg/kg at soil pH < 6.5 and 0.6 mg/kg at soil pH between 6.5 and 7.5 (SEPAC, 1995). It was clear that Cd concentrations in the soils from all of the three orchards exceeded the national soil standard. Therefore, the soils are not suitable for cultivation without remediation.
Total concentrations of Cd in soil samples are presented in
Table 1. The average concentration of Cd was 1.27, 1.84 and 0.68 mg/kg in orchards I, II and III, respectively. The soil Cd concentration in orchards I and II was approximately 1.9 and 2.7 times that in orchard III. The mean I-geo value (Table 1) was 2.52, 3.02 and 1.64 in orchards I, II, and III, respectively, suggesting that all three orchards were contaminated by Cd at different levels: moderate-severe (grade 3, orchard I), severe (grade 4, orchard II) and moderate (grade 2, orchard III). These results were probably due to the fact that these orchards used different irrigation water.
Rapid urbanization and industrialization has taken place in the areas surrounding the lower reaches of the Pearl River (the Pearl River Delta), including Guangzhou, since early 1980s. This rapid development has resulted in severe pollution of
the Pearl River (Liu et al., 2003; Chen et al., 2004; Ip et al.,
2004). Heavy metal levels in the surface sediment of the estuary have generally increased over the last two decades (Li et al., 2000). The maximum Cd concentration in the surface sediment reached 1.1 mg/kg and showed the highest
3.2. Cadmium accumulation in fruit trees and its potential health risk
Fig. 2 shows Cd concentrations in tissues of the three different species of fruit trees planted in orchard I. In the same tissue, Cd concentration in different species varied greatly. The highest Cd concentrations were observed in the carambola, and the lowest Cd concentrations generally occurred in the longan. The exceptionally high Cd concentrations in the root, 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 times of those of the longan, respectively. The foliar concentrations of Cd in both wampee and longan were within the normal range (0.1e2.4 mg/kg) of uncontaminated woody plants (Alloway, 1995). However, carambola foliar Cd (9.01 mg/kg) exceeded the normal range greatly. Moreover, among the three species studied, the carambola seemed to be the only species showing bio-accumulation of Cd, with tissue Cd levels greatly exceeding Cd levels in the associated soils. The bioaccumulation coefficient (7.0) was much higher than that found in Salix viminalis (0.83), a species known for its Cd accumulation capacity (Rosselli et al., 2003). Uptake and
Table 1 Selected properties of the orchard soils (mean Æ SD, n ¼ 10)
Orchard _
- Orchard II
- Orchard III
- pH
- 4.93Æ0.54 a*
19.69Æ13.28 b 25.41Æ9.77 b
1.27Æ0.45 b 0.66Æ0.41 a
5.16Æ0.31 a
12.35Æ5.36 b 22.11Æ10.65 b
1.84Æ0.73 a 0.72Æ0.33 a
39.71Æ13.77 a
3.02Æ0.48 a
4.11Æ0.13 b
30.36Æ9.04 a 36.98Æ5.48 a
0.68Æ0.14 c 0.05Æ0.02 b 7.57Æ1.32 b 1.64Æ0.28 c
OM content (g/kg) CEC (cmol/kg) Total Cd (mg/kg) DTPA-Cd (mg/kg) (DTPA-Cd)% I-geo
48.43Æ22.86 a
2.52Æ0.44 b
*Numbers followed by different letters in the same row indicate a significant difference (P < 0.05).
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A
B
Carambola Wampee a
Longan
0.30
16 14 12 10
8a
0.30
0.25 0.20 0.15
0.25 0.20 0.15 0.10 0.05 0.00 aa
a
6
0.10 bb
4b
- b
- b
- a
b
0.05
0.00 bb
2
b
- b
- b
b
0
- 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 different pathways, i.e., the root system and the foliar surface. Because Cd was below the detection limit (0.1 mg/L) in suspended particles in air samples collected from Guangzhou (Teng et al., 1999), and the plant samples were washed with tap and deionized water before digestion, it was unlikely that the high Cd concentrations in the carambola samples were the result of air-borne contamination. The high foliar Cd reflected a special ability of the carambola to accumulate Cd from soil. Therefore, the carambola might be considered as a Cd accumulator.
In general, Cd accumulators can transfer a large proportion of the pollutant from their roots to the above-ground tissues (Rosselli et al., 2003). In this work, the order of Cd accumulation in the carambola tissues (twig > leaf > root > fruit) was similar to that of the wampee (twig > root > leaf > fruit). Large proportions (74% in the carambola and 64% in the wampee) of total accumulated Cd in the plants were located in its above-ground tissues. The result was similar to the findings of Robinson et al. (2000) who reported that most Cd
(on dry weight basis) respectively. These results further demonstrated that the carambola tree had a special ability to accumulate Cd from soil and could be a Cd accumulator.
In China, the tolerance limit of cadmium in foods is
0.03 mg/kg (MHPRC, 1994). Cadmium in all three species of fruits (edible part) exceeded the tolerance limit more or less (Fig. 2). The carambola fruits from orchard I contained the highest Cd level (0.25 mg/kg, on a fresh weight basis), which was 8.4 times the tolerance limit. Cadmium concentrations in the carambola fruits obtained from orchard II (0.19 mg/kg) and orchard III (0.11 mg/kg), despite being lower than those in orchard I, were still much higher than the tolerance limit. These gave the carambola fruits a high average Tc (0.16), being much higher than those of the other two species (Fig. 2). The Tc of carambola fruits (edible part) was relatively high, and close to those of the vegetables with high Tc (Cui
et al., 2004), such as Apium graveolens L. (0.16) and Zingiber
officinale Rosc. (0.15). Such high Tc values indicate high potential health risks (US EPA, 1992). Therefore, among the three species of fruits, the carambola posed the highest potential health risk to local residents. According to the provisional tolerable weekly intake (PTWI) Cd values suggested by WHO (1989) (0.04 mg/day for a 40 kg child), a 40 kg child should not eat more than 0.16, 0.66, or 1.0 kg (on fresh weight basis) of the carambola, wampee or longan fruits from orchard I per day. During the harvesting season, the local residents on
´
(about 55%) accumulated by the poplar tree (Beaupre) sampled from a contaminated site in northern France was in the above-ground tissues (twigs and leaves). However, in the longan, only about 45% of the total Cd accumulated was in the above-ground tissues. The pattern of Cd distribution in the longan (root > twig > leaf > fruit) was typical of non-Cd accumulators, such as Mougeot Rowan (Rosselli et al., 2003) and Scotch pine (Kim et al., 2003).
Table 2 shows Cd concentrations in tissues of the carambola collected from different orchards. In the same tissue, Cd concentrations varied greatly among the orchards. Except for the root, carambola tissues collected from orchards I and orchard II contained significantly higher Cd levels than those from orchard III. However, high Cd bio-accumulation coeffi- cients were found in all three orchards (7.0 in orchard I, 4.6 in orchard II, and 5.8 in orchard III). The average Cd concentrations in twigs, leaves and fruits (edible part) of carambola trees from different orchards were 9.01, 7.16 and 1.56 mg/kg
Table 2 Cadmium concentration (mean Æ SD, n ¼ 10) in the carambola trees of the three orchards and Cd transfer coefficient (Tc) (edible part)
Orchard _
- Orchard II
- Orchard III
Root (mg/kg, dw) Twig (mg/kg, dw) Leaf (mg/kg, dw)
7.57Æ2.96
- e
- e
10.84Æ4.21 a* 10.97Æ5.27 a 5.23Æ1.04 b
- 9.01Æ2.98 a
- 8.54Æ4.26 a 4.03Æ1.41 b
1.64Æ0.44 b 0.92Æ0.25 c 0.19Æ0.05 b 0.11Æ0.03 c 0.11Æ0.05 b 0.16Æ0.03 b
Fruit(edible part) (mg/kg, dw) 2.15Æ0.51 a Fruit (edible part) (mg/kg, fw) 0.25Æ0.06 a
- Tc (edible part)
- 0.21Æ0.06 a
*Numbers followed by different letters in the same row indicate a significant difference (P < 0.05). e, data was unavailable.