Industrialization and urbanization have promoted socioeconomic development. However, they have also led to variety of environmental problems in peri-urban areas, such as agricultural soil contamination by heavy metals via various pathways. Commercial and residential vegetable growing areas are often located in the peri-urban areas for better market accessibility and higher prices (Smit 1996). Risk assessment of heavy metal contamination in vegetables in urban/peri-urban areas has been widely studied over recent decades (Singh and Kumar 2006). Lead and cadmium are considered as the most significant heavy metals affecting crops, and pose a great risk to human health via the consumption of vegetables. For example, the maximum level (ML) of Cd and Pb allowable in vegetable crops was set by the Commission of the European Communities (2006).

However, most of this research has focused on the total metal contents in vegetables and/or the metal fraction in soils (Fernandez-Turiel et al. 2001; Sterckeman et al. 2002; Douay et al. 2007; Kachenkom and Singhm 2006; Lim et al. 2008; Yan et al. 2007; Zheng et al. 2007). Are soils the sole contamination source for metal accumulation in plants? In fact, it has been confirmed that plants’ leaves can accumulate heavy metals from the atmosphere (Harrison and Chirgawi 1989; Temmerman and Hoenic 2004), thus the impacts of airborne heavy metals should not be neglected where atmospheric particles have high concentrations of heavy metals. The lead isotope ratio has been widely used to trace sources of metal pollution in the environment fields (Weiss et al. 1999; Hansmann and Koppel 2000; Ng et al. 2005; Cloquet et al. 2006; Erel et al. 2006; Komárek et al. 2008; Patrick and Farmer 2007). The lead isotope ratio in vegetables that originates from soils remains constant over time, and changes only if another source of lead with a different lead isotope ratio is introduced. In that case, the new lead isotopic content in vegetables will be a combination of the two lead sources, so it can indicate whether the surrounding soil was the sole source of contamination in the plants.

Nanjing, the capital of Jiangsu province, is a city with more than 2000 years of history, located in the lower reaches of the Yangtze River. Since the 1990s, Nanjing has been one of the fastest developing districts in industrialization and urbanization. Heavy metals contamination is a very serious problem (Zhang et al. 2005). Urban atmospheric Pb concentrations in Nanjing in winter and summer were 317 ± 28 and 200 ± 113 ng m−3, respectively (Mukai et al. 2001). The Qixiashan Lead–Zinc Mining/Smelting Plant (QLZMSP), located in the peri-urban area of Nanjing, has the largest lead–zinc deposit in East China. Approximately 350,000 tons of ore are treated per year, producing 50,000 tons of Zn and Pb. The unprotected mining wastes dispersed by wind and water, and atmospheric deposits of mining and smelting dust are important sources of pollution in the surrounding areas. In the present work, we investigated five popular leafy vegetables, two wild plants and the corresponding rhizospheric soils near the QLZMSP. Four leafy vegetables and the corresponding rhizospheric soils were also collected as controls from an area more distant from Nanjing. We aimed to assess Cd and Pb contamination in plants and corresponding soils in peri-urban and mining/smelting contaminated sites, and to elucidate the Pb contamination route for metal accumulation in plants through analysis of Pb isotope ratios.

Materials and Methods

Five popular vegetable species were collected from farmland approximately 100–200 m away from the QLZMSP (SI). The vegetables included pakchoi (Brassica chinensis L.), malabar spinach (Basella alba L.), celery (Apium graveolens L.), amaranth (Amaranthus spinosus L.), and lettuce (Lactuca sativa L.). Two wild plants were collected from the lawn at the QLZMSP (SII): Taraxacum mongolicum Hand.-Mazz and Rostellaria procumbens (L.) Nees. Farmland in Tangshan, approximately 5 km away from the QLZMSP, was selected as a control site (SIII). Four vegetables were collected from the control site; spinach (Spinacia oleracea Linn.), amaranth (Amaranthus spinosus L.), cole (Brassica campestris L.), and lettuce (Lactuca sativa L.). We collected 3–5 samples of each plant from each of the sites. The powdery remnant soils on the roots of plants were collected as the corresponding rhizospheric soil. The fresh vegetable samples were transported in clean plastic bags to the laboratory for further treatment as soon as possible. After being washed with tap water and Milli-Q water, each vegetable was separated into two parts; under-ground (roots) and above-ground (shoots). Plant material was dried in an electric drying oven at approximately 75°C. Soil samples were air-dried, crushed, and passed through a 0.15 mm-mesh sieve, then stored in polythene zip-bags at ambient temperature until further analysis.

Using a pH meter, soil pH was measured in 10 mM CaCl2 with a soil-to-solution ratio of 1:2.5 (w/v). Soil pH ranged from 6.7 to 7.4 for the studied rhizospheric soil. Triplicate soil samples were analyzed for metal content using aqua regia digestion (ISO 11466 (1995)). Two replicates of dry plant samples were digested with a HNO3–HClO4 mixture. Blanks for digestion and analysis methods and internal reference samples were carried out in triplicate with each set of samples. Precision and accuracy were verified using standard reference materials from the National Research Center for Geoanalysis, China (GBW07605 tea leaf). The recoveries were 98.5% for Pb and 91.2% for Cd. Water used for dilution and dissolution was purified using a Millipore deionizing system at 18.2 MΩ HCl, HNO3, and HClO4 were Suprapur reagents (Merck). Solutions from digested soil and plant samples were stored in 25 mL high density polyethylene samples bottles at 4°C until analysis. Lead and Cd were measured using a Perkin-Elmer ICP-MS SCIEX Elan 9000. The limits of detection for Pb and Cd were 0.005 and 0.002 μg L−1 in the present study. Lead isotopic analyses were conducted using a Perkin-Elmer ICP-MS SCIEX Elan 9000 as already described in the literature (Quétel et al. 1997; Bindler et al. 2004; Godoy et al. 2007). Precision and accuracy were verified using a standard reference material from the National Institute of Standards and Technology (SRM 981 common lead isotopic material). Repeated measurements of the SRM 981 Pb reference material over different analytical sessions showed uncertainties of <0.3% for 208Pb/206Pb and 206Pb/207Pb. Microsoft Excel (Ver. 2003) was used for data analysis in this study.

Results and Discussion

Concentrations of Cd and Pb in the studied rhizospheric soils are listed in Table 1. The order of concentrations of Pb and Cd in rhizospheric soil was SI > SII > SIII. Lead concentrations at the three sampling sites were all greater than background values in Nanjing district. Concentrations of Cd at SI and SII were greater than its background values. PPb was <1 at SII and SIII, but >1 at SI. However, Pi values for Cd all were >1 (Table 1). These results show that agricultural soils near the mining/smelting plant have been polluted with Pb and Cd. mining/smelting activities are the most important sources of heavy metals contaminating the environment. Fernandez-Turiel et al. (2001) found that metal concentrations were 31–8714 mg kg−1 for Pb, 0.27–30.68 mg kg−1 for Cd, 21–242 mg kg−1 for Cu, and 44–4637 mg kg−1 for Zn in soils located within the vicinity of a Pb smelter in Lastenia, Argentina. Sterckeman et al. (2002) reported that Cd, Pb, and Zn were the most abundant contaminants in the cultivated soils around two lead and zinc smelters. It was also reported that concentrations of heavy metals in soils decreased exponentially with distance from the mine source (Jung and Thornton 1996). Thus, heavy metals in soils at SI may be a combination of two or more sources. The lawn at the QLZMSP (SII) was sown approximately 5 years ago to beautify the plant, and the soil was taken from an area outside the plant. This may be one of the reasons why Pb and Cd concentrations at SII were lower than those at SI. The lowest concentrations of Pb and Cd were found in soils at SIII. Atmospheric deposition was the most important contamination source at the SIII sampling site. The background value of Cd in soils in the Nanjing district is above standards for soils environmental quality of People’s Republic of China, thus the soil contamination at SIII was not serious.

Table 1 Total concentration of Cd and Pb in the rhizospheric soils (mg kg−1)
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The contents of heavy metals in the shoots and roots of vegetables are listed in Table 2. Contents of Cd and Pb varied greatly among the various vegetable species. The order of concentrations of Pb and Cd in shoots and roots was SII > SI > SIII. There were significant differences in Pb and Cd contents in plants among the three sampling sites. Pb and Cd contents in vegetables at SI and SII were much higher than those in vegetable collected from SIII. Maximum levels for Pb and Cd in brassicas and leaf vegetables are 0.30 and 0.20 mg kg−1 wet weight, respectively, in (EC) No 1881/2006. The conversion factor 0.085 was used to convert fresh green vegetable weight to dry weight, as described by Rattan et al. (2005). The maximum levels for Pb and Cd in this study were therefore approximately 3.53 and 2.35 mg kg−1 dry weight. Pb and Cd concentrations of the vegetables’ edible parts (shoots) were all beyond their maximum levels at SI, and below maximum levels at SIII. This result indicated that vegetables around the plant were heavily polluted with Cd and Pb and posed a great risk to consumers. This result also suggests that heavy metals contamination in vegetables caused by mining/smelting activities is more serious than urban atmospheric depositions.

Table 2 Concentrations of Cd and Pb in shoots and roots of plants (mg kg−1 dw) and enrichment coefficients from root to shoot
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The shoot/root ratio of Cd and Pb contents showed that the tissue distribution of Cd and Pb varied greatly among various vegetable species (Table 2). The shoot/root ratio of Cd in lettuce was approximately twice that in celery at SI. At SI the shoot/root ratio of Pb in lettuce was 0.22, whereas it was approximately seven times higher in malabar spinach (1.55). High values of shoot/root ratio indicated that more metal was accumulated in shoots. It is consistent with the findings of Zheng et al. (2007) and Lim et al. (2008). Generally, metal content in shoots were less than those roots of plants growing in an unpolluted-air area (Finster et al. 2004; Deng et al. 2004; Sharma and Dubey 2005). These observations suggest that the impact of airborne heavy metals should not be neglected where atmospheric particles have high concentrations of heavy metals.

Figure 1 shows Pb isotope ratios in shoots of plants and soils at the three sampling sites. Pb isotope ratios in shoots of plants and soils at SI and SII were clearly different to those at SIII. This may be because SI and SII are exposed to metal contamination from both urban atmospheric transport and from mining/smelting dust deposition, whereas SII is only exposed to contamination from urban atmospheric transport. There was a clear distinction in Pb isotope ratios between soils and shoots of plants (Fig. 1). Pb isotope ratios in shoots of plants at SI and SII were similar. They had high 208/206Pb values, compared to the corresponding soils. Values of 208/206Pb and 206/207Pb in shoots of vegetables at SIII were also higher than those in the corresponding soils. If no new sources of Pb with different Pb isotope ratios were introduced, the lead isotope ratios in plants should be similar to those in the corresponding soils. The Pb stable isotope ratios in vegetables indicated that there was a combination of two or more Pb sources. This result indicated that soils were not the sole contamination source for metal accumulation in plants. Airborne Pb may be the other source of contamination in plants in peri-urban and mining/smelting sites in the present study. It has been confirmed that plants’ leaves can accumulate heavy metals from the atmosphere (Harrison and Chirgawi 1989; Voutsa et al. 1996; Temmerman and Hoenic 2004). Thus, the Pb isotopic content in plants is possibly a combination of soilborne Pb uptaken through the soil-to-root pathway, and airborne Pb assimilated via the atmosphere-to-leaf pathway.

Fig. 1
figure 1

Pb isotope ratios in shoots of plants and the corresponding soils at the three sampling sites

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