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Transfer of cadmium and lead from soil to mangoes in an uncontaminated area, Hainan Island, China
Geoderma 155 (2010) 115–120
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Geoderma j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / g e o d e r m a
Transfer of cadmium and lead from soil to mangoes in an uncontaminated area, Hainan Island, China Xiangyang Bi a,b,⁎, Limin Ren a,b, Min Gong b, Yusheng He c, Lei Wang d, Zhendong Ma b a
Key Laboratory of Biogeology and Environmental Geology, Ministry of Education, Wuhan 430074, PR China Faculty of Earth Science, China University of Geosciences, Wuhan 430074, PR China Hainan Geological Survey, Haikou 570206, PR China d Faculty of Earth Resources, China University of Geosciences, Wuhan 430074, PR China b c
a r t i c l e
i n f o
Article history: Received 11 August 2009 Received in revised form 1 December 2009 Accepted 8 December 2009 Available online 4 January 2010 Keywords: Cadmium Lead Soil Mangoes Transfer factors Atomic absorption spectroscopy
a b s t r a c t Exposure to toxic metals from fruits is an important pathway of human exposure to soil pollutants, but few researches on metals accumulation in the soil–fruit system were performed. In this study, we conducted a systemic survey of Cd and Pb accumulations in the soil–mango (Mangifera indica L.) system from an uncontaminated area, Hainan Island, China. Results indicated that concentrations of Cd and Pb in the soil were controlled by the parent materials, with concentrations ranging from 0.019–0.21 μg g− 1 for Cd and 8– 63 μg g− 1 for Pb in total and from 0.003–0.059 μg g− 1 for Cd and 0.8–7.0 μg g− 1 for Pb in labile fractions, respectively. The concentrations of Cd and Pb in the mango fruits showed ranges of 0.3–4.2 and 0.8–209 ng g− 1 (FW), respectively, which varied significantly between cultivars. The transfer factors (TFs) of metals from soil to fruit showed significant differences between cultivars, from 0.01 to 0.025 for Cd and from 0.001 to 0.0019 for Pb. The ANOVA and correlation analyses indicated that the variations of metal in the fruit depended on the difference of cultivars, while the variations of metal concentrations within cultivar were controlled, to some extent, by the soil metal levels. Our finding suggests that the use of the individual cultivar to assess the soil metal bioavailability or metal transfer ability from soil to plant may be more precise than the use of different cultivars. Quantitative chemical analysis was performed using flame or graphite furnace atomic absorption spectroscopy. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Cadmium (Cd) and lead (Pb) are nonessential elements for humans, which can cause various acute and chronic adverse effects, such as renal, nervous, and osseous diseases (WHO, 1992, 1995; McLaughlin et al., 1999; Koller et al., 2004; Satarug and Moore, 2004; Williams et al., 2009) and were identified as carcinogen to humans (IARC, 1993, 2006). Previous studies indicated that exposure even at low levels, these metals can generate a harmful effect to human (Koller et al., 2004; Satarug and Moore, 2004). Therefore for a better protection of human health, it is necessary to understand and control the levels of Cd and Pb in foodstuffs. As one of the most important foodstuffs, fruits contain a lot of biologically active substances, such as antioxidants, anticancerogens, antimutagens, and antibacterial compounds (Bobrowska-Grzesik and Jakóbik-Kolon, 2008, and references therein). With respect to healthy effects on human, fruits may also contain and cumulate a toxic level of metals (McLaughlin et al., 1999; Li et al., 2006). However, studies on toxic metals accumulation in fruits are not sufficient compared to other foodstuffs, such as vegetables and field crops (McLaughlin et al., ⁎ Corresponding author. Tel./fax: +86 27 87055853. E-mail address: [email protected] (X. Bi). 0016-7061/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.geoderma.2009.12.004
1999). Few data for toxic metals in fruits previously reported were mainly from polluted area (Ward and Savage, 1994; Li et al., 2006) or from the market (Jorhem and Sundström, 1993; Sanchez-Castillo et al., 1998; Karavoltsos et al., 2002; Parveen et al., 2003; Radwan and Salama, 2006; Karavoltsos et al., 2008). The information of metals accumulation in fruits in uncontaminated areas is scarce. Among the previous studies, Ward and Savage (1994) have reviewed Cd and Pb concentrations for “uncontaminated” fruits. Pillay et al. (2002) studied Cd accumulation in dates from a relatively clean area of Oman, later they published the baseline values of another 11 metals (Ag, Al, Ba, Be, Ga, La, Mo, Se, Si, Tl, and V) in dates from the same area (Williams et al., 2005). Consuming the edible plants contaminated by the metals transferred from soil is an important pathway of human exposure to environmental contaminants. The transfer factor (TF) impacted especially by the soil properties and plant species (McLaughlin et al., 1999), may play an important role and is usually considered as a useful index of the metals potentially transfer abilities from soil to plant (Wang et al., 2006). Currently, TFs have been widely used in the evaluation of the potential health risk of human exposure to metals from soil (Chojnacka et al., 2005; Li et al., 2006; Wang et al., 2006; Green and Tibbett, 2008; Williams et al., 2009).
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In this study, we firstly conducted a systemic geochemical survey of orchard soil and mango (Mangifera indica L.) in an uncontaminated area, Hainan Island, southern China, and aimed to (1) present the levels of Cd and Pb concentrations in mango fruit; (2) determine influences of soil metal concentrations and the cultivar difference on the accumulations of Cd and Pb in the fruit; (3) delineate the transfer characteristic of Cd and Pb from soil to mango regarding different cultivars.
semi-weathering parent materials were collected for comparison with the soil samples. After sampling, soil samples were air-dried at room temperature (25 °C), and ground to b100 μm. Plant samples were thoroughly cleaned with tap water and Milli-Q water to remove adhering particles, and then the edible parts were separated and dried in an oven at 60 °C. The dry samples were weighed for calculation of the water content and ground to fine powder for chemical analysis.
2. Materials and methods 2.3. Analytical methods 2.1. Description of the study area The study area, Hainan Island, is located in southern China (18°10′– 20°10′N, 108°37′–111°03′E) and covers 33,920 km2 of land area (Fig. 1). The central Five Finger Mountain is the highest mountain in the island with an altitude of 1867 m above sea level. Climate in this area is tropical monsoon with average annual rainfall of 1600–2500 mm and average annual temperature of 23–25 °C. The main soil types in Hainan are cambosols and ferrosols on the parent materials of acid igneous rocks, cambosols on clastic sediments, ferralosols on basic igneous rocks, and primosols and cambosola on marine sediments. In the study area, mango, banana, and pineapple are the main fruit productions with average annual outputs of 0.26, 1.08, and 0.21 million tons, respectively. 2.2. Sampling and preparation The sampling campaign was carried out in May 2006. Sixty-seven samples of mango (M. indica L.) fruits were collected (Fig. 1). Each sample was comprised of 5–10 sub-samples. The sampled mango trees were from three native cultivars (Ji-Dan, Tai-Nong, and Xiang-Ya). The soil samples were directly collected from under the sampled plants and consisted of at least 5 sub-samples. Thirteen parent materials or
Soil pH was determined in a 2.5:1 water/soil suspension using a pH meter (LY/T, 1239-1999). Soil organic matter (OM) content was determined by potassium dichromate method (LY/T, 1237-1999). For Cd and Pb determinations in the soil, 0.2 g thoroughly homogenized samples were weighed into 50 ml Teflon vessels, then added 5 ml 30% HCl, 5 ml 65% HNO3, 4 ml 40% HF and 2 ml 70% HClO4 and heated on a hot plate until near dryness. After cooling, the residue was redissolved in 2 ml 65% HNO3 and diluted to 25 ml with Milli-Q water (GB/T, 171411997). For fruit analysis, 1 g homogenized samples were weighed into 50 ml Pyrex beakers and decomposed with 10 ml 65% HNO3 and 4 ml 30% H2O2 on a hot plate. After cooling, the residual suspension was filtered in a 25-ml volumetric flask and diluted to the mark (GB/T 5009.12-2003; GB/T 5009.15-2003). Readily labile fractions of Cd and Pb from the orchard soils were estimated by extraction of 10.0 g of soil with 50 ml 0.1 mol L− 1 hydrochloric acid (LY/T, 1260-1999). The concentrations of Pb and Cd in the digests were determined using flame or graphite furnace atomic absorption spectrometry (PE-800, Perkin-Elmer Inc.). For quality assurance and quality control (QA/QC), we analyzed duplicates, method blanks and standard reference materials (GBW 07404 and GBW 07602). Mean recoveries for soil were within 100 ± 10%, and for plant were within 100 ± 20%. Method blanks in each batch of samples were negligible.
Fig. 1. Study area and sampling locations (from Google Earth).
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2.4. Data analysis 2.4.1. Transfer factors The transfer factors (TFs) of Cd and Pb from soil to fruit (edible part) were calculated using the following equation (Chojnacka et al., 2005; Li et al., 2006; Wang et al., 2006; Green and Tibbett, 2008; Williams et al., 2009): TF =
Cfruit Csoil
where Cfruit refers to Cd or Pb concentration (FW) in fruit, and Csoil is Cd or Pb concentration (DW) in the soil where the fruit tree was grown. 2.4.2. Statistical analysis The data statistical analysis was performed using statistical package, SPSS 11.0 for Windows (SPSS Inc., USA). Correlation analysis between Cd and Pb concentrations in samples of soils and mangoes was performed using the Pearson correlation procedure. Statistical significance of differences in both sample concentrations of Cd and Pb and TF values was computed using one-way ANOVA. 3. Results and discussion 3.1. Cd and Pb in orchard soils The total Cd concentrations in soils ranged from 0.019 to 0.21 μg g− 1, with a high mean value of 0.20 μg g− 1 in soils derived from limestone (Table 1). For Pb, the mean total concentrations ranged from 25 μg g− 1 on acid igneous rock to 55 μg g− 1 on limestone (Table 1). These values are comparable to those of Cd and Pb in arable soils not subject to gross anthropogenic pollution, which were generally 0.1–2 μg g− 1 and 20– 50 μg g− 1, respectively (McLaughlin et al., 1999). The significant correlations (p b 0.001) of metal concentrations between the soils and parent materials shown in Fig. 2, indicated that Cd and Pb in the Hainan orchard soils were mainly controlled by the parent materials. But Cd and Pb showed different behaviors in the supergene environment. The similar concentrations and distribution trends of Pb between soils and parent materials indicated the steady nature of Pb during the weathering process (Fig. 2), while Cd was quite mobile and preferred to enrich in soils compared to the parent materials as shown by Fig. 2. These results suggested that the Hainan orchard soils had not suffered obvious contamination. On average, 23% (0.018 μg g− 1) of the total Cd in Hainan orchard soils was labile, while Pb was comparatively unmovable and only 12% (3.9 μg g− 1) of the total Pb was readily labile (Table 1).
Fig. 2. Relationships of total Cd and Pb concentrations between orchard soils and parent materials.
Table 1 Cd and Pb concentrations and selected properties of the orchard soils and parent materials. Parent material types
Acid igneous rock Marine sediment Clastic sediment Limestone Total
Parent material
Soil
Cd⁎
Pb
Cd
T
T
T
L
T
L
0.072b⁎⁎ (0.04–0.09) 0.058b (0.05–0.07) 0.072b (0.05–0.09) 0.125a (0.11–0.14) 0.077 (0.04–0.14)
42a (30–57) 30a (15–43) 28a (24–32) 48a (37–59) 38 (15–59)
0.072b (0.02–0.14) 0.075b (0.019–0.16) 0.088b (0.066–0.11) 0.20a (0.18–0.21) 0.079 (0.019–0.21)
0.018a (0.004–0.059) 0.018a (0.011–0.024) 0.014a (0.003–0.025) 0.025a (0.02–0.03) 0.018 (0.003–0.059)
32b (14–45) 26b (8–45) 25b (24–26) 55a (48–63) 32 (8–63)
4.5a (1.6–7.0) 3.5a (3.0–3.8) 3.7a (3.1–4.3) 2.6a (0.8–4.3) 3.9 (0.8–7.0)
T: Total concentration (μg g− 1); L: Labile fraction concentration (μg g− 1). ⁎Levels are presented in mean and range values (in parenthesis). ⁎⁎Numbers followed by different letters indicate a significant difference (p b 0.05).
Pb
OM (%)
pH
1.4a (0.4–2.2) 1.4a (0.5–2.9) 1.1a (0.6–1.5) 1.8a (1.7–1.8) 1.4 (0.4–2.9)
6.0a (4.8–7.0) 5.8a (4.4–7.3) 5.2b (4.8–5.6) 6.0a (5.9–6.0) 6.0 (4.4–7.3)
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Table 2 Cd and Pb concentrations (ng g− 1, FW) in mango fruits and the TF values. Cultivars
Cd⁎ N
Ji-Dan Tai-Nong Xiang-Ya Total
19 24 24 67
Pb Concentration a⁎⁎
(0.40–4.2) 1.27 1.15a (0.30–2.9) b 0.68 (0.30–1.3) 1.0 (0.30–4.2)
TF
N ab
0.013 0.025a 0.010b 0.016
(0.005–0.04) (0.004–0.15) (0.004–0.02) (0.004–0.15)
Concentration b
19 24 24 67
33 (12–85) 26b (0.8–100) 65a (4.6–209) 42 (0.8–209)
TF 0.0010b 0.0010b 0.0019a 0.0013
(0.0003–0.0038) (0.0001–0.0044) (0.0003–0.0039) (0.0001–0.0044)
⁎ Levels are presented in mean and range values (in parenthesis). ⁎⁎ Numbers followed by different letters indicate a significant difference (p b 0.05).
3.2. Cd and Pb in mango fruits The range of Cd concentrations in the mango fruits was 0.30– 4.2 ng g− 1 (FW), with a mean value of 1.0 ng g− 1. For Pb, the concentrations varied from 0.8 to 209 ng g− 1, with a mean value of 42 ng g− 1 (Table 2). Among the three cultivars (Ji-Dan, Tai-Nong, and Xiang-Ya) in this study, the Ji-Dan and Tai-Nong cultivars contained significantly higher Cd concentrations compared to Xiang-Ya cultivar, which had the highest Pb concentrations (mean 65 ng g− 1) (Table 2). The concentrations of Cd and Pb in arboreal fruits in some other parts of the world are presented in Table 3. Comparison with data of mango and other fruits recorded in Pakistan (Parveen et al., 2003), Mexico (Sanchez-Castillo et al., 1998) and Guangzhou, China (Li et al., 2006), Cd and Pb levels in our study were considerably low (Table 3). The range of mango Cd levels in our study was similar to that found in Egypt (Radwan and Salama, 2006), Greece (Karavoltsos et al., 2002), Sweden (Jorhem and Sundström, 1993), and Brazil (Santos et al., 2004). However, Pb concentrations in some mango samples in this study were beyond the ranges reported in Egypt (Radwan and Salama, 2006), Greece (Karavoltsos et al., 2008), Brazil (Santos et al., 2004), and Turkey (Yaman et al., 2000) (Table 3). In order to safeguard the human dietary exposure to toxicity metals, maximum contaminant levels (MCLs) have been set for various foods. In China the upper limit for Cd and Pb in fruits are 50 and 100 ng g− 1 (FW), respectively (GB, 2762-2005). Compared to
these national standards, Cd concentrations in all mango samples in this study were less than the MCLs. However, Pb in 7% (five out of 67) of the samples failed to meet the MCLs, and most of these high Pb level samples belonged to Xiang-Ya cultivar. 3.3. Relationships between Cd and Pb concentrations in orchard soils and in mango fruits The correlation analysis based on total concentrations revealed that Cd and Pb in the mango fruits of Ji-Dan and Tai-Nong cultivars were not significantly correlated (p N 0.05) with their concentrations in soil, respectively. However, a significantly positive correlation (p b 0.001) was found for Pb concentrations between soils and the mango fruits of Xiang-Ya cultivar (Fig. 3), which can be described by a linear equation: y = 3:220x−36:362 where y is the Pb concentration in the fruit of Xiang-Ya mango, x refers to total soil Pb concentration. This reflected the dominant control of soil Pb on the Pb concentrations in these mango samples. Moreover, it is worth estimating from this model that N42 μg Pb g− 1 in soil may induce Pb levels in the Xiang-Ya mango fruit beyond the MCL value (100 ng g− 1). Hence the area with soil Pb concentrations above 42 μg g− 1 in Hainan may not be suitable for
Table 3 Comparison of Cd and Pb concentrations in fruits between mango from Hainan and published data from other parts of the world. Locations
Fruit types
Cd (ng g− 1)a
Pb (ng g− 1)
Reference
Egypt (DW)
Apple Date Grapefruit Peach Orange Apple Mango Apple Pear Apple Pear Mango Apple Lime Lemon Mamey Orange Plum Soursop Apple Orange Apple Orange Carambola Mango (DW) (FW)
50 (20–70) 10 (1–19) 2 (1–3) 10 (8–15) 40 (10–80) 140 270 b 1 (b 1–1) 6 (4–8)
190 (170–220) 220 (130–290) 160 (120–230) 380 (260–470) 150 (70–250) 760 1510 b5 (b 5–5) 6 50–75 150 240 360 370 410 730 240 (280–330) 220 4.4 (0.02–27) 21 (9.0–44) 12.9 27.2
Radwan and Salama (2006)
Pakistan (DW) Sweden (DW) Turkey (DW) Mexico (FW)
Brazil (FW) Greece (FW) Guangzhou, China (FW) Hainan, China
a
Levels are presented in mean and range values (in parenthesis).
0.3 (b 0.008–9.2) 0.1 (b 0.03–0.3) 0.3 (0.2–0.6) 0.9 (0.2–1.9) 190–250 9.0 (2.6–37) 1.0 (0.30–4.2)
Parveen et al. (2003) Jorhem and Sundström (1993) Yaman et al. (2000) Sanchez-Castillo et al. (1998)
Santos et al. (2004) Karavoltsos et al. (2002, 2008) Li et al. (2006) This study
370 (7.0–1840) 42 (0.8–209)
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Fig. 3. Relationships between total Cd and Pb concentrations in orchard soils and Cd and Pb concentrations in mango fruits.
planting Xiang-Ya mango. Similarly, the Cd concentrations in the fruit of Xiang-Ya mango were also significantly positive (p b 0.001) correlated to the soil Cd (Fig. 3). But this relationship was restricted to situations where soil Cd concentrations were not greater than 0.11 μg g− 1. When the soil Cd levels were above 0.11 μg g− 1, the concentrations of Cd in mango were not increased with increasing soil Cd concentrations (Fig. 3). This might suggest a physiological mechanism for exclusion of Cd from seed generating organs. Such an exclusion mechanism of Cd has been reported for other plant species (Harris and Taylor, 2001; Green and Tibbett, 2008). The relationships based on liable concentrations showed that the correlations between liable soil Cd and Cd in Ji-Dan mango fruits and between liable soil Pb and Pb in Tai-Nong mango fruits were at statistical significant levels (Fig. 4). When results for all three mango cultivars were combined, there were no such significant relationships of Cd and Pb between soil and mango fruit (Figs. 3 and 4). This suggested that the variations of metal concentrations in mango fruits were not controlled by soil metals but by the genotypes or/and the plant physiology. While the above significant relationships indicated that the variations of metal concentrations within cultivar depended, to some extent, on the soil metal levels. 3.4. Transfer factors of Cd and Pb from soil to mango The transfer factors (TFs) of Cd from soil to fruit based on total soil concentrations for the three cultivars of mango varied from 0.004 to 0.15 (Table 2). The TF values (mean 0.028) of Cd in the Tai-Nong cultivar were significantly higher than those of the Xiang-Ya mango (mean 0.01), suggesting a high ability of Cd uptaking and translocation. The lowest TF values of Cd (mean 0.01) in Xiang-Ya mango may
again reflect the exclusion mechanism of Cd from fruit in the plant. The TF values of Pb were ranging from 0.0001 to 0.0044 and for XiangYa mango (mean 0.0019) were significantly higher than those of the Ji-Dan and Tai-Nong mango (both mean 0.001), suggesting that the Xiang-Ya mango would take up and translocate more soil Pb than the other two cultivars. However, the TF values of Pb were an order of magnitude lower than that of Cd. It might reflect that Pb is much more difficult to be transferred from the soils into the mango fruits than Cd, which was in agreement with other works (Wang et al., 2006; Williams et al., 2009). We obtained the TF data of Cd for carambola, wampee and longan cultivated in an urban area of Guangzhou, south China (Li et al., 2006), of which the values (0.11–0.21) were much higher than those of our study. However, the TF values of Cd and Pb for mango in this study were similar to those reported for leafy vegetables (0.005–0.34 and 0.0002–0.0048 for Cd and Pb, respectively) from southeastern China (Wang et al., 2006), suggesting that they had the similar uptake ability for Cd and Pb in soils. The TFs of metals for a given plant depend on the metal nature in soil (e.g. concentration and chemical fractions) and the physiological mechanism (metal uptake and translocation mechanism) of plant. The significant positive correlations between Cd and Pb concentrations in mango fruits and TF values of Cd and Pb suggested that the TF values of Cd and Pb depended on the fruit metal concentrations (Table 4). This is most likely to be influenced by the plant physiological factors. In addition, the TF values of Cd for Tai-Nong and Xiang-Ya mango and TF values of Pb for Tai-Nong mango were significantly negatively correlated to their corresponding soil Cd and Pb concentrations (Table 4), indicating that the TF values of Cd and Pb in these cases were also affected by soil metal concentrations.
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our study may be a valuable reference for future similar study. In addition, this study can offer valuable information for local government to adjust farming policy. Acknowledgements This study was supported by the China Geological Survey (2006010002) and the Natural Science Foundation of China (40703023 and 40703020). References
Fig. 4. Relationships between liable Cd and Pb concentrations in orchard soils and Cd and Pb concentrations in mango fruits.
4. Conclusions This study presented Cd and Pb accumulations in mango fruits of different cultivars grown in a relatively uncontaminated area. Results indicated that Cd concentrations in mango fruits were far more below the MCL value, while Pb concentrations in 7% of the mango fruit samples exceeded the MCL value. The significant linear model between Pb concentration in Xiang-Ya mango and soil suggests that the soil with Pb concentration higher than 42 μg g− 1 may result in a Pb level in Xiang-Ya mango fruit beyond the MCL value, and is therefore not suitable for the planting of this mango cultivar. The TFs reflect the uptake ability of mango for soil metals and may depend, in this study, mainly on the physiological mechanism of the mango plants, but in some cases, the soil metal concentrations were also important. Our finding suggests that the use of the individual cultivar to assess the soil metal bioavailability or soil to plant metal transfer ability may be more precise than the use of different cultivar. Since the data about metal accumulated in fruit plants were relatively scarce, Table 4 Pearson correlation between TF values and Cd and Pb concentrations in orchard soils and mango fruits. Cd
TF-Cd Ji-Dan Tai-Nong Xiang-Ya
Pb
Soil
Fruit
–0.110 − 0.557⁎⁎ − 0.451⁎
0.920⁎⁎ 0.752⁎⁎ 0.290
⁎ Significant level at p b 0.05. ⁎⁎ p b 0.01 (two-tailed).
TF-Pb Ji-Dan Tai-Nong Xiang-Ya
Soil
Fruit
− 0.404 − 0.513⁎ 0.335
0.894⁎⁎ 0.777⁎⁎ 0.823⁎⁎
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Geoderma j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / g e o d e r m a
Transfer of cadmium and lead from soil to mangoes in an uncontaminated area, Hainan Island, China Xiangyang Bi a,b,⁎, Limin Ren a,b, Min Gong b, Yusheng He c, Lei Wang d, Zhendong Ma b a
Key Laboratory of Biogeology and Environmental Geology, Ministry of Education, Wuhan 430074, PR China Faculty of Earth Science, China University of Geosciences, Wuhan 430074, PR China Hainan Geological Survey, Haikou 570206, PR China d Faculty of Earth Resources, China University of Geosciences, Wuhan 430074, PR China b c
a r t i c l e
i n f o
Article history: Received 11 August 2009 Received in revised form 1 December 2009 Accepted 8 December 2009 Available online 4 January 2010 Keywords: Cadmium Lead Soil Mangoes Transfer factors Atomic absorption spectroscopy
a b s t r a c t Exposure to toxic metals from fruits is an important pathway of human exposure to soil pollutants, but few researches on metals accumulation in the soil–fruit system were performed. In this study, we conducted a systemic survey of Cd and Pb accumulations in the soil–mango (Mangifera indica L.) system from an uncontaminated area, Hainan Island, China. Results indicated that concentrations of Cd and Pb in the soil were controlled by the parent materials, with concentrations ranging from 0.019–0.21 μg g− 1 for Cd and 8– 63 μg g− 1 for Pb in total and from 0.003–0.059 μg g− 1 for Cd and 0.8–7.0 μg g− 1 for Pb in labile fractions, respectively. The concentrations of Cd and Pb in the mango fruits showed ranges of 0.3–4.2 and 0.8–209 ng g− 1 (FW), respectively, which varied significantly between cultivars. The transfer factors (TFs) of metals from soil to fruit showed significant differences between cultivars, from 0.01 to 0.025 for Cd and from 0.001 to 0.0019 for Pb. The ANOVA and correlation analyses indicated that the variations of metal in the fruit depended on the difference of cultivars, while the variations of metal concentrations within cultivar were controlled, to some extent, by the soil metal levels. Our finding suggests that the use of the individual cultivar to assess the soil metal bioavailability or metal transfer ability from soil to plant may be more precise than the use of different cultivars. Quantitative chemical analysis was performed using flame or graphite furnace atomic absorption spectroscopy. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Cadmium (Cd) and lead (Pb) are nonessential elements for humans, which can cause various acute and chronic adverse effects, such as renal, nervous, and osseous diseases (WHO, 1992, 1995; McLaughlin et al., 1999; Koller et al., 2004; Satarug and Moore, 2004; Williams et al., 2009) and were identified as carcinogen to humans (IARC, 1993, 2006). Previous studies indicated that exposure even at low levels, these metals can generate a harmful effect to human (Koller et al., 2004; Satarug and Moore, 2004). Therefore for a better protection of human health, it is necessary to understand and control the levels of Cd and Pb in foodstuffs. As one of the most important foodstuffs, fruits contain a lot of biologically active substances, such as antioxidants, anticancerogens, antimutagens, and antibacterial compounds (Bobrowska-Grzesik and Jakóbik-Kolon, 2008, and references therein). With respect to healthy effects on human, fruits may also contain and cumulate a toxic level of metals (McLaughlin et al., 1999; Li et al., 2006). However, studies on toxic metals accumulation in fruits are not sufficient compared to other foodstuffs, such as vegetables and field crops (McLaughlin et al., ⁎ Corresponding author. Tel./fax: +86 27 87055853. E-mail address: [email protected] (X. Bi). 0016-7061/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.geoderma.2009.12.004
1999). Few data for toxic metals in fruits previously reported were mainly from polluted area (Ward and Savage, 1994; Li et al., 2006) or from the market (Jorhem and Sundström, 1993; Sanchez-Castillo et al., 1998; Karavoltsos et al., 2002; Parveen et al., 2003; Radwan and Salama, 2006; Karavoltsos et al., 2008). The information of metals accumulation in fruits in uncontaminated areas is scarce. Among the previous studies, Ward and Savage (1994) have reviewed Cd and Pb concentrations for “uncontaminated” fruits. Pillay et al. (2002) studied Cd accumulation in dates from a relatively clean area of Oman, later they published the baseline values of another 11 metals (Ag, Al, Ba, Be, Ga, La, Mo, Se, Si, Tl, and V) in dates from the same area (Williams et al., 2005). Consuming the edible plants contaminated by the metals transferred from soil is an important pathway of human exposure to environmental contaminants. The transfer factor (TF) impacted especially by the soil properties and plant species (McLaughlin et al., 1999), may play an important role and is usually considered as a useful index of the metals potentially transfer abilities from soil to plant (Wang et al., 2006). Currently, TFs have been widely used in the evaluation of the potential health risk of human exposure to metals from soil (Chojnacka et al., 2005; Li et al., 2006; Wang et al., 2006; Green and Tibbett, 2008; Williams et al., 2009).
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In this study, we firstly conducted a systemic geochemical survey of orchard soil and mango (Mangifera indica L.) in an uncontaminated area, Hainan Island, southern China, and aimed to (1) present the levels of Cd and Pb concentrations in mango fruit; (2) determine influences of soil metal concentrations and the cultivar difference on the accumulations of Cd and Pb in the fruit; (3) delineate the transfer characteristic of Cd and Pb from soil to mango regarding different cultivars.
semi-weathering parent materials were collected for comparison with the soil samples. After sampling, soil samples were air-dried at room temperature (25 °C), and ground to b100 μm. Plant samples were thoroughly cleaned with tap water and Milli-Q water to remove adhering particles, and then the edible parts were separated and dried in an oven at 60 °C. The dry samples were weighed for calculation of the water content and ground to fine powder for chemical analysis.
2. Materials and methods 2.3. Analytical methods 2.1. Description of the study area The study area, Hainan Island, is located in southern China (18°10′– 20°10′N, 108°37′–111°03′E) and covers 33,920 km2 of land area (Fig. 1). The central Five Finger Mountain is the highest mountain in the island with an altitude of 1867 m above sea level. Climate in this area is tropical monsoon with average annual rainfall of 1600–2500 mm and average annual temperature of 23–25 °C. The main soil types in Hainan are cambosols and ferrosols on the parent materials of acid igneous rocks, cambosols on clastic sediments, ferralosols on basic igneous rocks, and primosols and cambosola on marine sediments. In the study area, mango, banana, and pineapple are the main fruit productions with average annual outputs of 0.26, 1.08, and 0.21 million tons, respectively. 2.2. Sampling and preparation The sampling campaign was carried out in May 2006. Sixty-seven samples of mango (M. indica L.) fruits were collected (Fig. 1). Each sample was comprised of 5–10 sub-samples. The sampled mango trees were from three native cultivars (Ji-Dan, Tai-Nong, and Xiang-Ya). The soil samples were directly collected from under the sampled plants and consisted of at least 5 sub-samples. Thirteen parent materials or
Soil pH was determined in a 2.5:1 water/soil suspension using a pH meter (LY/T, 1239-1999). Soil organic matter (OM) content was determined by potassium dichromate method (LY/T, 1237-1999). For Cd and Pb determinations in the soil, 0.2 g thoroughly homogenized samples were weighed into 50 ml Teflon vessels, then added 5 ml 30% HCl, 5 ml 65% HNO3, 4 ml 40% HF and 2 ml 70% HClO4 and heated on a hot plate until near dryness. After cooling, the residue was redissolved in 2 ml 65% HNO3 and diluted to 25 ml with Milli-Q water (GB/T, 171411997). For fruit analysis, 1 g homogenized samples were weighed into 50 ml Pyrex beakers and decomposed with 10 ml 65% HNO3 and 4 ml 30% H2O2 on a hot plate. After cooling, the residual suspension was filtered in a 25-ml volumetric flask and diluted to the mark (GB/T 5009.12-2003; GB/T 5009.15-2003). Readily labile fractions of Cd and Pb from the orchard soils were estimated by extraction of 10.0 g of soil with 50 ml 0.1 mol L− 1 hydrochloric acid (LY/T, 1260-1999). The concentrations of Pb and Cd in the digests were determined using flame or graphite furnace atomic absorption spectrometry (PE-800, Perkin-Elmer Inc.). For quality assurance and quality control (QA/QC), we analyzed duplicates, method blanks and standard reference materials (GBW 07404 and GBW 07602). Mean recoveries for soil were within 100 ± 10%, and for plant were within 100 ± 20%. Method blanks in each batch of samples were negligible.
Fig. 1. Study area and sampling locations (from Google Earth).
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2.4. Data analysis 2.4.1. Transfer factors The transfer factors (TFs) of Cd and Pb from soil to fruit (edible part) were calculated using the following equation (Chojnacka et al., 2005; Li et al., 2006; Wang et al., 2006; Green and Tibbett, 2008; Williams et al., 2009): TF =
Cfruit Csoil
where Cfruit refers to Cd or Pb concentration (FW) in fruit, and Csoil is Cd or Pb concentration (DW) in the soil where the fruit tree was grown. 2.4.2. Statistical analysis The data statistical analysis was performed using statistical package, SPSS 11.0 for Windows (SPSS Inc., USA). Correlation analysis between Cd and Pb concentrations in samples of soils and mangoes was performed using the Pearson correlation procedure. Statistical significance of differences in both sample concentrations of Cd and Pb and TF values was computed using one-way ANOVA. 3. Results and discussion 3.1. Cd and Pb in orchard soils The total Cd concentrations in soils ranged from 0.019 to 0.21 μg g− 1, with a high mean value of 0.20 μg g− 1 in soils derived from limestone (Table 1). For Pb, the mean total concentrations ranged from 25 μg g− 1 on acid igneous rock to 55 μg g− 1 on limestone (Table 1). These values are comparable to those of Cd and Pb in arable soils not subject to gross anthropogenic pollution, which were generally 0.1–2 μg g− 1 and 20– 50 μg g− 1, respectively (McLaughlin et al., 1999). The significant correlations (p b 0.001) of metal concentrations between the soils and parent materials shown in Fig. 2, indicated that Cd and Pb in the Hainan orchard soils were mainly controlled by the parent materials. But Cd and Pb showed different behaviors in the supergene environment. The similar concentrations and distribution trends of Pb between soils and parent materials indicated the steady nature of Pb during the weathering process (Fig. 2), while Cd was quite mobile and preferred to enrich in soils compared to the parent materials as shown by Fig. 2. These results suggested that the Hainan orchard soils had not suffered obvious contamination. On average, 23% (0.018 μg g− 1) of the total Cd in Hainan orchard soils was labile, while Pb was comparatively unmovable and only 12% (3.9 μg g− 1) of the total Pb was readily labile (Table 1).
Fig. 2. Relationships of total Cd and Pb concentrations between orchard soils and parent materials.
Table 1 Cd and Pb concentrations and selected properties of the orchard soils and parent materials. Parent material types
Acid igneous rock Marine sediment Clastic sediment Limestone Total
Parent material
Soil
Cd⁎
Pb
Cd
T
T
T
L
T
L
0.072b⁎⁎ (0.04–0.09) 0.058b (0.05–0.07) 0.072b (0.05–0.09) 0.125a (0.11–0.14) 0.077 (0.04–0.14)
42a (30–57) 30a (15–43) 28a (24–32) 48a (37–59) 38 (15–59)
0.072b (0.02–0.14) 0.075b (0.019–0.16) 0.088b (0.066–0.11) 0.20a (0.18–0.21) 0.079 (0.019–0.21)
0.018a (0.004–0.059) 0.018a (0.011–0.024) 0.014a (0.003–0.025) 0.025a (0.02–0.03) 0.018 (0.003–0.059)
32b (14–45) 26b (8–45) 25b (24–26) 55a (48–63) 32 (8–63)
4.5a (1.6–7.0) 3.5a (3.0–3.8) 3.7a (3.1–4.3) 2.6a (0.8–4.3) 3.9 (0.8–7.0)
T: Total concentration (μg g− 1); L: Labile fraction concentration (μg g− 1). ⁎Levels are presented in mean and range values (in parenthesis). ⁎⁎Numbers followed by different letters indicate a significant difference (p b 0.05).
Pb
OM (%)
pH
1.4a (0.4–2.2) 1.4a (0.5–2.9) 1.1a (0.6–1.5) 1.8a (1.7–1.8) 1.4 (0.4–2.9)
6.0a (4.8–7.0) 5.8a (4.4–7.3) 5.2b (4.8–5.6) 6.0a (5.9–6.0) 6.0 (4.4–7.3)
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Table 2 Cd and Pb concentrations (ng g− 1, FW) in mango fruits and the TF values. Cultivars
Cd⁎ N
Ji-Dan Tai-Nong Xiang-Ya Total
19 24 24 67
Pb Concentration a⁎⁎
(0.40–4.2) 1.27 1.15a (0.30–2.9) b 0.68 (0.30–1.3) 1.0 (0.30–4.2)
TF
N ab
0.013 0.025a 0.010b 0.016
(0.005–0.04) (0.004–0.15) (0.004–0.02) (0.004–0.15)
Concentration b
19 24 24 67
33 (12–85) 26b (0.8–100) 65a (4.6–209) 42 (0.8–209)
TF 0.0010b 0.0010b 0.0019a 0.0013
(0.0003–0.0038) (0.0001–0.0044) (0.0003–0.0039) (0.0001–0.0044)
⁎ Levels are presented in mean and range values (in parenthesis). ⁎⁎ Numbers followed by different letters indicate a significant difference (p b 0.05).
3.2. Cd and Pb in mango fruits The range of Cd concentrations in the mango fruits was 0.30– 4.2 ng g− 1 (FW), with a mean value of 1.0 ng g− 1. For Pb, the concentrations varied from 0.8 to 209 ng g− 1, with a mean value of 42 ng g− 1 (Table 2). Among the three cultivars (Ji-Dan, Tai-Nong, and Xiang-Ya) in this study, the Ji-Dan and Tai-Nong cultivars contained significantly higher Cd concentrations compared to Xiang-Ya cultivar, which had the highest Pb concentrations (mean 65 ng g− 1) (Table 2). The concentrations of Cd and Pb in arboreal fruits in some other parts of the world are presented in Table 3. Comparison with data of mango and other fruits recorded in Pakistan (Parveen et al., 2003), Mexico (Sanchez-Castillo et al., 1998) and Guangzhou, China (Li et al., 2006), Cd and Pb levels in our study were considerably low (Table 3). The range of mango Cd levels in our study was similar to that found in Egypt (Radwan and Salama, 2006), Greece (Karavoltsos et al., 2002), Sweden (Jorhem and Sundström, 1993), and Brazil (Santos et al., 2004). However, Pb concentrations in some mango samples in this study were beyond the ranges reported in Egypt (Radwan and Salama, 2006), Greece (Karavoltsos et al., 2008), Brazil (Santos et al., 2004), and Turkey (Yaman et al., 2000) (Table 3). In order to safeguard the human dietary exposure to toxicity metals, maximum contaminant levels (MCLs) have been set for various foods. In China the upper limit for Cd and Pb in fruits are 50 and 100 ng g− 1 (FW), respectively (GB, 2762-2005). Compared to
these national standards, Cd concentrations in all mango samples in this study were less than the MCLs. However, Pb in 7% (five out of 67) of the samples failed to meet the MCLs, and most of these high Pb level samples belonged to Xiang-Ya cultivar. 3.3. Relationships between Cd and Pb concentrations in orchard soils and in mango fruits The correlation analysis based on total concentrations revealed that Cd and Pb in the mango fruits of Ji-Dan and Tai-Nong cultivars were not significantly correlated (p N 0.05) with their concentrations in soil, respectively. However, a significantly positive correlation (p b 0.001) was found for Pb concentrations between soils and the mango fruits of Xiang-Ya cultivar (Fig. 3), which can be described by a linear equation: y = 3:220x−36:362 where y is the Pb concentration in the fruit of Xiang-Ya mango, x refers to total soil Pb concentration. This reflected the dominant control of soil Pb on the Pb concentrations in these mango samples. Moreover, it is worth estimating from this model that N42 μg Pb g− 1 in soil may induce Pb levels in the Xiang-Ya mango fruit beyond the MCL value (100 ng g− 1). Hence the area with soil Pb concentrations above 42 μg g− 1 in Hainan may not be suitable for
Table 3 Comparison of Cd and Pb concentrations in fruits between mango from Hainan and published data from other parts of the world. Locations
Fruit types
Cd (ng g− 1)a
Pb (ng g− 1)
Reference
Egypt (DW)
Apple Date Grapefruit Peach Orange Apple Mango Apple Pear Apple Pear Mango Apple Lime Lemon Mamey Orange Plum Soursop Apple Orange Apple Orange Carambola Mango (DW) (FW)
50 (20–70) 10 (1–19) 2 (1–3) 10 (8–15) 40 (10–80) 140 270 b 1 (b 1–1) 6 (4–8)
190 (170–220) 220 (130–290) 160 (120–230) 380 (260–470) 150 (70–250) 760 1510 b5 (b 5–5) 6 50–75 150 240 360 370 410 730 240 (280–330) 220 4.4 (0.02–27) 21 (9.0–44) 12.9 27.2
Radwan and Salama (2006)
Pakistan (DW) Sweden (DW) Turkey (DW) Mexico (FW)
Brazil (FW) Greece (FW) Guangzhou, China (FW) Hainan, China
a
Levels are presented in mean and range values (in parenthesis).
0.3 (b 0.008–9.2) 0.1 (b 0.03–0.3) 0.3 (0.2–0.6) 0.9 (0.2–1.9) 190–250 9.0 (2.6–37) 1.0 (0.30–4.2)
Parveen et al. (2003) Jorhem and Sundström (1993) Yaman et al. (2000) Sanchez-Castillo et al. (1998)
Santos et al. (2004) Karavoltsos et al. (2002, 2008) Li et al. (2006) This study
370 (7.0–1840) 42 (0.8–209)
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Fig. 3. Relationships between total Cd and Pb concentrations in orchard soils and Cd and Pb concentrations in mango fruits.
planting Xiang-Ya mango. Similarly, the Cd concentrations in the fruit of Xiang-Ya mango were also significantly positive (p b 0.001) correlated to the soil Cd (Fig. 3). But this relationship was restricted to situations where soil Cd concentrations were not greater than 0.11 μg g− 1. When the soil Cd levels were above 0.11 μg g− 1, the concentrations of Cd in mango were not increased with increasing soil Cd concentrations (Fig. 3). This might suggest a physiological mechanism for exclusion of Cd from seed generating organs. Such an exclusion mechanism of Cd has been reported for other plant species (Harris and Taylor, 2001; Green and Tibbett, 2008). The relationships based on liable concentrations showed that the correlations between liable soil Cd and Cd in Ji-Dan mango fruits and between liable soil Pb and Pb in Tai-Nong mango fruits were at statistical significant levels (Fig. 4). When results for all three mango cultivars were combined, there were no such significant relationships of Cd and Pb between soil and mango fruit (Figs. 3 and 4). This suggested that the variations of metal concentrations in mango fruits were not controlled by soil metals but by the genotypes or/and the plant physiology. While the above significant relationships indicated that the variations of metal concentrations within cultivar depended, to some extent, on the soil metal levels. 3.4. Transfer factors of Cd and Pb from soil to mango The transfer factors (TFs) of Cd from soil to fruit based on total soil concentrations for the three cultivars of mango varied from 0.004 to 0.15 (Table 2). The TF values (mean 0.028) of Cd in the Tai-Nong cultivar were significantly higher than those of the Xiang-Ya mango (mean 0.01), suggesting a high ability of Cd uptaking and translocation. The lowest TF values of Cd (mean 0.01) in Xiang-Ya mango may
again reflect the exclusion mechanism of Cd from fruit in the plant. The TF values of Pb were ranging from 0.0001 to 0.0044 and for XiangYa mango (mean 0.0019) were significantly higher than those of the Ji-Dan and Tai-Nong mango (both mean 0.001), suggesting that the Xiang-Ya mango would take up and translocate more soil Pb than the other two cultivars. However, the TF values of Pb were an order of magnitude lower than that of Cd. It might reflect that Pb is much more difficult to be transferred from the soils into the mango fruits than Cd, which was in agreement with other works (Wang et al., 2006; Williams et al., 2009). We obtained the TF data of Cd for carambola, wampee and longan cultivated in an urban area of Guangzhou, south China (Li et al., 2006), of which the values (0.11–0.21) were much higher than those of our study. However, the TF values of Cd and Pb for mango in this study were similar to those reported for leafy vegetables (0.005–0.34 and 0.0002–0.0048 for Cd and Pb, respectively) from southeastern China (Wang et al., 2006), suggesting that they had the similar uptake ability for Cd and Pb in soils. The TFs of metals for a given plant depend on the metal nature in soil (e.g. concentration and chemical fractions) and the physiological mechanism (metal uptake and translocation mechanism) of plant. The significant positive correlations between Cd and Pb concentrations in mango fruits and TF values of Cd and Pb suggested that the TF values of Cd and Pb depended on the fruit metal concentrations (Table 4). This is most likely to be influenced by the plant physiological factors. In addition, the TF values of Cd for Tai-Nong and Xiang-Ya mango and TF values of Pb for Tai-Nong mango were significantly negatively correlated to their corresponding soil Cd and Pb concentrations (Table 4), indicating that the TF values of Cd and Pb in these cases were also affected by soil metal concentrations.
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our study may be a valuable reference for future similar study. In addition, this study can offer valuable information for local government to adjust farming policy. Acknowledgements This study was supported by the China Geological Survey (2006010002) and the Natural Science Foundation of China (40703023 and 40703020). References
Fig. 4. Relationships between liable Cd and Pb concentrations in orchard soils and Cd and Pb concentrations in mango fruits.
4. Conclusions This study presented Cd and Pb accumulations in mango fruits of different cultivars grown in a relatively uncontaminated area. Results indicated that Cd concentrations in mango fruits were far more below the MCL value, while Pb concentrations in 7% of the mango fruit samples exceeded the MCL value. The significant linear model between Pb concentration in Xiang-Ya mango and soil suggests that the soil with Pb concentration higher than 42 μg g− 1 may result in a Pb level in Xiang-Ya mango fruit beyond the MCL value, and is therefore not suitable for the planting of this mango cultivar. The TFs reflect the uptake ability of mango for soil metals and may depend, in this study, mainly on the physiological mechanism of the mango plants, but in some cases, the soil metal concentrations were also important. Our finding suggests that the use of the individual cultivar to assess the soil metal bioavailability or soil to plant metal transfer ability may be more precise than the use of different cultivar. Since the data about metal accumulated in fruit plants were relatively scarce, Table 4 Pearson correlation between TF values and Cd and Pb concentrations in orchard soils and mango fruits. Cd
TF-Cd Ji-Dan Tai-Nong Xiang-Ya
Pb
Soil
Fruit
–0.110 − 0.557⁎⁎ − 0.451⁎
0.920⁎⁎ 0.752⁎⁎ 0.290
⁎ Significant level at p b 0.05. ⁎⁎ p b 0.01 (two-tailed).
TF-Pb Ji-Dan Tai-Nong Xiang-Ya
Soil
Fruit
− 0.404 − 0.513⁎ 0.335
0.894⁎⁎ 0.777⁎⁎ 0.823⁎⁎
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