HEAVY METALS CONTAMINATION IN VEGETABLES GROWN IN URBAN AND METAL SMELTER CONTAMINATED SITES IN AUSTRALIA

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1 HEAVY METALS CONTAMINATION IN VEGETABLES GROWN IN URBAN AND METAL SMELTER CONTAMINATED SITES IN AUSTRALIA ANTHONY GEORGE KACHENKO and BALWANT SINGH Faculty of Agriculture, Food and Natural Resources, Ross Street Building A03, The University of Sydney, New South Wales 2006, Australia ( author for correspondence, akac1808@mail.usyd.edu.au, Tel , Fax: ) (Received 11 November 2004; accepted 28 July 2005) Abstract. Dietary exposure to heavy metals, namely cadmium (Cd), lead (Pb), zinc (Zn) and copper (Cu), has been identified as a risk to human health through the consumption of vegetable crops. This study investigates the source and magnitude of heavy metal contamination in soil and vegetable samples at 46 sites across four vegetable growing regions in New South Wales, Australia. The four regions Boolaroo, Port Kembla, Cowra and the Sydney Basin were a mix of commercial and residential vegetable growing areas. The extent of metal contamination in soils sampled was greatest in regions located in the vicinity of smelters, such as in Boolaroo and Port Kembla. Soil metal concentrations decreased with depth at these two sites, suggesting contamination due to anthropogenic activities. Cadmium, Pb and Zn contamination was greatest in vegetables from Boolaroo, and Cu concentrations were greatest in vegetables sampled from Port Kembla. At Boolaroo, nearly all the samples exceeded the Australian Food Standards maximum level (ML) (0.01 mg kg 1 fresh weight) of Cd and Pb in vegetables. Over 63% of samples exceeded international food standard guidelines set by the Commission of the European Communities and the Codex Alimentarius Commission. All vegetables sampled from Cowra, which is a relatively pristine site had Cd and Pb levels below the Australian and international food standards guideline values. This study suggests that the Australian guideline values are more conservative in defining the ML for Cd and Pb in vegetable crops. This investigation highlights the increased danger of growing vegetables in the vicinity of smelters. Keywords: contamination, transfer coefficients, guidelines, heavy metals, uptake 1. Introduction The implications associated with metal (embracing metalloids) contamination is of great concern, particularly in agricultural production systems. Metals most often found as contaminants in vegetables include As, Cd and Pb. These metals can pose as a significant health risk to humans, particularly in elevated concentrations above the very low body requirements (Gupta and Gupta, 1998). The contamination of agricultural soils is often a direct or indirect consequence of anthropogenic activities (McLaughlin et al., 1999). Sources of anthropogenic metal contamination in soils include - urban and industrial wastes; mining and smelting of non ferrous metals and metallurgical industries (Singh, 2001). Commercial Water, Air, and Soil Pollution (2006) 169: C Springer 2006

2 102 A. G. KACHENKO AND B. SINGH and residential vegetable growing areas are often located in urban areas, and are subject to anthropogenic contamination. Fernandez Turiel et al. (2001) found elevated levels of heavy metals in urban soils located within the vicinity of a Pb smelter in Lastenia, Argentina. The heavy metals found at elevated concentrations were Pb ( mg kg 1 ), Cd ( mg kg 1 ), Cu ( mg kg 1 ) and Zn ( mg kg 1 ). A study of urban soil contamination by Beavington (1973) found elevated levels of Cu (343 mg kg 1 )inthe industrial area of Wollongong, New South Wales (NSW), Australia. Other sources of anthropogenic contamination include the addition of manures, sewage sludge, fertilizers and pesticides to soils, with a number of studies identifying the risks in relation to increased soil metal concentration and consequent crop uptake (Whatmuff, 2002; McBride, 2003). Both commercial and residential growing areas are also subject to atmospheric pollution, in the form of metal containing aerosols. These aerosols can enter the soil and be absorbed by vegetables, or alternatively be deposited on leaves and adsorbed. Studies of vegetables grown in locations close to industry have reported elevated levels of heavy metals. Vousta et al. (1996) studied the impact of atmospheric pollution from industry on heavy metal contamination in vegetables grown in Greece. The results of the study indicated significantly higher levels of metal accumulation in leafy vegetables as compared with root vegetables. This partitioning of Cd is well known, with accumulation of greater concentrations in the edible leafy portions of crops, than the storage organs or fruit (Jinadasa et al., 1997; Lehoczky et al., 1998). Both Cd and Pb are considered as the most significant heavy metals affecting vegetable crops. In Australia and New Zealand, the maximum level (ML) of Cd and Pb allowable in vegetable crops has been set by the Australian and New Zealand Food Authority (ANZFA) (ANSTAT, 2001). For Cd the ML is 0.1 mg kg 1 fresh weight (FW) for all vegetable types. The ML of Pb is also 0.1 mg kg 1 FW for all vegetable types excluding Brassicas (0.3 mg kg 1 FW). The Commission of the European Communities (2001) and the Codex Alimentarius Commission (2001, 2004) sets similar levels of Cd and Pb for vegetable crops. Both organisations set the ML for Cd as 0.2 mg kg 1 FW for leafy vegetables and fresh herbs, 0.1 mg kg 1 for stem and root vegetables and 0.05 mg kg 1 for the remaining ungrouped vegetables. For Pb, both organizations set the ML of 0.3 mg kg 1 FW for brassicas, leafy vegetables and herbs, and 0.1 mg kg 1 FW for all remaining vegetables. The level of Cd in vegetables of commercial growing regions located within the Sydney Basin has been extensively studied (Jinadasa et al., 1997). To our knowledge, there are no systematic published studies on metals contamination in Australian vegetable growing regions, particularly in urban and metal smelter contaminated sites. In this study we investigated the concentrations of As, Cd, Cu, Pb and Zn in both soil and vegetable crops within vegetable growing regions of NSW, Australia; and evaluated their contamination status with respect to Australian and international food standard guidelines.

3 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA 103 Figure 1. Location of sampling regions. 2. Materials and Methods 2.1. SAMPLING SITES Soil and plant samples were collected from 46 sites within four regions across NSW, Australia (Figure 1). There were 24 sites sampled in the Sydney Basin, 11 in Boolaroo, 6 in Port Kembla and 5 in the Cowra region. The sites were a mixture of commercial vegetable farms and private residential vegetable gardens. The regions of Boolaroo and Port Kembla (both residential) were within close proximity to industrial sites. The region of Boolaroo is located 140 km north of Sydney, NSW. The region was host to a Pb Zn smelter located in the centre of Boolaroo which had been in operation since 1897, ceasing operations in September Tam and Singh (2004) suggested that the smelter is the primary source of soil heavy metal contamination in the immediate region surrounding the smelter. The region of Port Kembla is situated 80 km south of Sydney, NSW, and was home to a Cu smelter (which ceased operation in July 2003), steelworks and fertilizer plant among other smaller industry. Previous studies have indicated soil contamination, primarily in the nearby urban areas surrounding the Cu smelter (Beavington, 1973). At Port Kembla and Boolaroo, sampling sites were within a 3 km radius of the smelter and representative of soil metal concentrations observed in previous studies. The remaining two regions, Sydney Basin (residential and commercial) and Cowra (commercial) have no obvious point source of pollution. The sites in the Sydney Basin are located in the metropolitan city of Sydney and may have diffused pollution from manufacturing industries, the application of sewage sludge and other waste

4 104 A. G. KACHENKO AND B. SINGH materials. The agricultural region of Cowra is located approximately 300 km west of Sydney and has minimal contamination from anthropogenic sources, and can be considered as relatively pristine SOIL AND PLANT SAMPLING A total of 113 soil samples and 138 plant samples were collected from 46 sites in the four regions. A transect of 5 5mwas selected at random at each site from which both soil and vegetable samples were collected. From each transect two composite soil samples were collected with a stainless steel auger, at 0 30 cm (n = 69) and at cm (n = 44) depths. Each composite soil sample (1 kg) was taken from 5 thoroughly mixed subsamples taken at random locations within the transect. At commercial vegetable growing sites two transects were sampled to account for site variability among soil samples. At the second transect only topsoil samples were collected. Soil texture varied from sand to loam, sandy clay loam to heavy clay. According to The Australian Soil Classification system (Isbell, 1996), soils in the Boolaroo region included Brown/Yellow Chromosols, Yellow Kandosols and Brown/Yellow Dermosols. Soils sampled in Cowra comprised of Red/Brown Chromosols and Red/Brown Dermosols and from Port Kembla included Brown Chromosols and Brown Dermosols. Greatest variation in soil types was observed in soils sampled from the Sydney Basin, and included; Red/Brown Chromosols, Yellow Brown Dermosols, Aeric Podosols, Yellow Brown Kandosols and Yellow Brown Kurosols. The edible portions of 2 plants (e.g. leafy, root, fruit) were randomly sampled from each transect. Leafy vegetables were preferred for sampling since past research shows that they accumulate heavy metals at a greater capacity than other vegetables (Jinadasa et al., 1997; Lehoczky et al., 1998). The number of plant samples collected from the Sydney Basin was 82, from Boolaroo 22, Port Kembla 18, and Cowra 16 (Table II). The vegetables sampled include 56 lettuce (Lactuca sativa L.), 44 spinach (Spinacia oleracea L.), 8 cabbage (Brassica oleracea L.), 6 leek (Allium porrum L.), 4 rhubarb (Rheum rhabarbarum L.) and 2 beetroot (Beta vulgaris). Herbs sampled included 14 parsley (Petroselinum crispum var. crispum) and 4 mint (Mentha spicata L.) SOIL ANALYSIS The soil samples were air-dried, mechanically ground using a stainless steel roller and sieved to obtain <2 mmfraction. A g subsample was drawn from the bulk soil (<2 mm fraction) and reground to obtain <200 µm fraction using a mortar and pestle. This fine material was used to determine organic carbon, cation exchange capacity (CEC) and total metal content in soil. The <2mmfraction was used to determine ph (1:5 soil water extract), electrical conductivity (EC) (1:5 soil water extract) and particle size analysis using methods outlined by Rayment

5 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA 105 and Higginson (1992). Organic carbon was determined by the modified Walkley and Black method (dichromate oxidation and titration) (McCleod, 1975); cation exchange capacity by the 0.01 M silver-thiourea method (Rayment and Higginson, 1992). Soil samples were digested in a mixture of concentrated nitric acid (HNO 3 ), concentrated hydrochloric acid (HCl) and 27.5% hydrogen peroxide (H 2 O 2 ) according to the USEPA Method 3050B (USEPA, 1996) for the analysis of heavy metals (As, Cd, Cu, Pb and Zn). The extracts were analysed using a Vista Varian inductively coupled plasma atomic emission spectrometer (ICP-AES). The detection limit for As was 0.1 mg kg 1, for Pb it was 0.02 mg kg 1 and 0.01 mg kg 1 for Cd, Zn and Cu. A graphite furnace atomic absorption spectrometer (Vista Varian Spectra 220Z) was used to verify Cd concentrations <0.5 mg kg PLANT ANALYSIS The plant samples were put through a three step washing sequence, which involved agitating and rinsing first in 0.1% teepol for 15 seconds, followed by 0.1% HCl for 15 seconds and lastly three separate washes in deionised water (Reuter et al., 1988). The clean vegetable samples were air dried, weighed and placed in a dehydrator at 70 C for hours depending on sample size. Dried samples were weighed and mechanically ground using a stainless steel grinder (<1 mm) for digestion. A portion of the dry vegetable powder material was digested in a mixture of HNO 3 and perchloric acid (HClO 4 ) (Miller, 1998). As with soil samples, the extracts were analysed for various elements using ICP-AES, and Cd using a graphite furnace atomic absorption spectrometer (Vista Varian Spectra 220Z) ANALYTICAL QUALITY Three certified reference soils and two reference plant materials were digested in a similar manner to the contaminated samples for quality control and to monitor any instrument variability. The reference soils included San Joaquin with baseline trace element concentrations, GBW and Montana 2710 with high trace element concentrations. The analysed values for the certified samples were lower than the certified values. The certified values are based on the complete dissolution of the samples and the USEPA method 3050B does not completely dissolve soil, which leads to lower analysed values. Results of the acid digestions indicate 86% of Cu, 83% of Zn, 80% of Cd and 70% of Pb was recovered from certified reference soils. The two certified reference plant materials, pine needles and peach leaves were uncontaminated and contained low levels of most metals, with no highly contaminated plant standards to make comparison. Results for the acid digestions indicate 90% of Pb and 100% of Cd, Cu and Zn was recovered from certified reference plant materials.

6 106 A. G. KACHENKO AND B. SINGH 2.6. STATISTICAL ANALYSIS Statistical analysis was performed by using Genstat version (Payne, 2002). Soil and plant data were not normally distributed and were log transformed prior to statistical analysis. Statistically significant differences were determined using residual maximum likelihood (REML) regression analysis. The analysis constructs least square means from the effects fitted to explore relationships established in the analysis. The least square means refer to the modelled means (predicted means) calculated through the REML analysis. In addition, correlations were calculated to measure the degree of linear relationship between plant metal concentrations and soil properties/soil metal concentrations. 3. Results and Discussion 3.1. GENERAL SOIL PROPERTIES Soil ph in water varied between the four regions (P < 0.001), with little differences observed between topsoil and subsoil values (Table I). The mean topsoil and subsoil ph ranged from strongly acidic (4.04) to strongly alkaline (9.22) for all soils sampled. Electrical conductivity also varied significantly between the four regions (P < 0.01), with higher means for topsoil layers than the subsoil layers (P < 0.001). The overall EC values ranged from 71 µs cm 1 in subsoil from Boolaroo to 1020 µscm 1 in topsoil from the Sydney Basin (Table I). A majority of EC values suggest non-saline growing conditions in the studied regions. Soil organic carbon (%) differed between regions (P < 0.001) and was greatest in the topsoil, decreasing with depth at all four regions (P < 0.001) (Table I). The mean topsoil organic carbon content was greatest at Boolaroo (3.6 ± 1.4) followed by Port Kembla (3.4 ± 1.2), Sydney Basin (2.0 ± 1.1) and least in soils from Cowra (0.9 ± 0.34). The same trend was observed for subsoil organic carbon across the four regions. Clay content (%) did not significantly differ between regions, however it increased significantly with depth at all four regions (P < 0.001) (Table I). The mean topsoil clay content was greatest in the Sydney Basin (21.0 ± 10.3), and least in the Boolaroo region (12.1 ± 3.6). The same trend was observed between the regions in relation to subsoil clay content. Cation exchange capacity (mmol c kg 1 )was generally very low across all regions (Table I). There was considerable variation between regions ( P < 0.001) and between soil layers (P < 0.01). The CEC was lowest in both topsoil (63 ± 11) and subsoil (63 ± 8) from Cowra, and highest in both topsoil (155 ± 29) and subsoil (156 ± 59) from Port Kembla. At Boolaroo, the difference between topsoil and subsoil CEC was greatest in comparison with the remaining three regions.

7 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA 107 TABLE I Geometric mean (±SD) and range of cadmium, copper, lead and zinc in vegetables sampled Cowra Boolaroo Sydney Basin Port Kembla Topsoil Subsoil Topsoil Subsoil Topsoil Subsoil Topsoil Subsoil (0 30 cm) (60 90 cm) (0 30 cm) (60 90 cm) (0 30 cm) (60 90 cm) (0 30 cm) (60 90 cm) ph (1:5 H2O) Mean ± SD 7.27 ± ± ± ± ± ± ± ± 0.56 Median Range EC (µscm 1 ) Mean ± SD 265 ± ± ± ± ± ± ± ± 282 Median Range Organic carbon (%) Mean ± SD 0.9 ± ± ± ± ± ± ± ± 0.61 Median Range Clay (%) Mean ± SD 17.6 ± ± ± ± ± ± ± ± 17.3 Median Range CEC (mmolc kg 1) Mean ± SD 63 ± ± ± ± ± ± ± ± 59 Median Range Free Fe content (%) Mean ± SD 1.57 ± ± ± ± ± ± ± ± 2.28 Median Range

8 108 A. G. KACHENKO AND B. SINGH Free Fe content (%) was greatest in subsoils from Port Kembla (5.48 ± 2.28), and least in subsoils from Cowra (1.53±0.37). There was a significant difference in free Fe between regions (P < 0.001), however this variation was no seen between soil layers (P = 0.239) for each region TOTAL ELEMENT ANALYSIS OF SOIL The level of heavy metals in the soils was compared to the National Environmental Protection (Assessment of Site Contamination) Measures set by the National Environment Protection Council (NEPC, 1999). The guideline builds on the Australian and New Zealand Guidelines for the assessment and management of contaminated sites (Australia and New Zealand Environmental and Conservation Council, 1992), in recognising a balance between the use of soil criteria and site-specific assessment. The guidelines identify ecological investigation levels (EILs), based on total metal concentration, considerations of phytotoxicity (Cu, Cr and Pb), Australia and New Zealand Environment and Conservation Council B levels and soil survey data from urban residential properties in four Australian capital cities Cadmium The highest Cd concentrations in soil were observed at Boolaroo (Figure 2a), where Cd values ranged from 0.01 mg kg 1 (subsoil) to mg kg 1 (topsoil). Of the 22 soils sampled, 50% exceeded the 3 mg kg 1 EIL (NEPC, 1999). Tam and Singh (2004) also found elevated Cd concentrations in soils from the Boolaroo region, with concentrations ranging between mg kg 1. The Cd levels from the topsoils at Boolaroo were significantly higher ( P < 0.001) than the Cd levels found in the topsoils at Port Kembla, Sydney Basin and Cowra regions. Elevated Cd concentrations were also found at Port Kembla. The values ranged from 0.01 (subsoil) to 7.01 mg kg 1 (topsoil), with a median value of 1.37 mg kg 1.Ofthe 16 soils sampled, 5 exceeded the EIL. Cadmium content in most soils from Boolaroo and Port Kembla were greater than the reported range for Australian soils ( mg kg 1 )(Williams and David, 1973), however within the normal range ( mg kg 1 ) reported for the worlds soils (Sanchez-Camazano et al., 1994). These values suggest anthropogenic sources of contamination, which is further supported by significantly high levels of soil Cd in topsoils, than subsoils at both regions ( P < 0.001). At Boolaroo topsoil and subsoil mean concentrations were 5.54 and 0.11 mg kg 1, respectively. These findings are lower than those of Sterckeman et al. (2000) who found elevated Cd levels in surface horizons (up to 305 mg kg 1 ) and subsurface horizons (up to 14 mg kg 1 )insoils near smelters of northern France. The higher Cd concentrations in their study are likely a result of there being 2 smelters, a Zn smelter and a Pb Zn smelter 3.5 km apart, in the area from which they sampled. Lower concentrations of Cd were found at Port Kembla, the mean topsoil and subsoil Cd concentration were 1.22 and 0.14 mg kg 1, respectively. This may be due to the difference in smelting activity at both regions.

9 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA 109 Figure 2. Regional least square means (mg kg 1 DW) of(a) cadmium, (b) copper, (c) lead, (d) zinc and (e) arsenic for topsoil and subsoil layers. The magnitude of the standard error for the least square means are indicated by the error bars. The ecological investigation levels (EILs) are indicated by broken lines.

10 110 A. G. KACHENKO AND B. SINGH The Cd concentrations in both the Sydney Basin and Cowra regions were significantly lower than at Boolaroo and Port Kembla ( mg kg 1 ) (Figure 2a). The Cd concentrations in all soils sampled from these regions were under the 3mgkg 1 EIL. Most of the values fall within the range reported for Australian soils ( mg kg 1 )(Williams and David, 1973), and the normal range ( mg kg 1 ) reported for the worlds soils (Sanchez-Camazano et al., 1994). An earlier study by Jinadasa et al. (1997) surveyed 29 commercial vegetable operations throughout the Sydney Basin. They found similar levels of soil Cd ranging from 0.2 to 1.99 mg kg 1, with a median value of 0.04 mg kg 1, and a mean of 0.36 mg kg 1. Across all regions, positive linear correlations existed between soil Cd and organic carbon (r = 0.482) and CEC (r = 0.371). These correlations may explain the elevated Cd concentrations in the topsoils sampled from all regions. Soil Cd concentrations were also strongly associated with soil Zn concentrations (r = 0.842). This relation was also identified by Jinadasa et al. (1997) who found a significant interaction between Cd and Zn (r = 0.510) in soils sampled across the greater Sydney Basin. They suggest that the Cd-contaminated Zn compounds used for agricultural use, foliar sprays or poultry manure applications were the likely sources of contamination Copper The highest Cu levels were observed in soils from the Port Kembla region (Figure 2b), with values ranging between 65 (subsoil) to 1032 (topsoil) mg kg 1.Of the 16 samples investigated, 75% exceeded the NEPC (1999) EIL of 100 mg kg 1. Soil Cu decreased significantly with depth ( P < 0.001), with the mean topsoil and subsoil concentrations of 338 and 173 mg kg 1, respectively. Soil Cu concentrations at Port Kembla were significantly different from those found at Boolaroo, Sydney Basin and Cowra ( P < 0.001). Similar levels were reported by Beavington (1973) who found elevated soil Cu levels (mean value of 343 mg kg 1 ) within a 1 km radius of the smelting plant in Port Kembla. He also found that levels of Cu in the urban areas extending beyond this 1 km radius were elevated, and Cu content in soils decreased with depth; the mean topsoil (0 30 cm) and subsoil (30 60 cm) values of these urban areas were and 15.7 mg kg 1, respectively. Similarly Gundermann and Hutchinson (1995) found elevated levels of Cu within a 2 km radius of a Ni Cu smelter in North America, with levels decreasing at distance from the smelter. These findings identify the smeltering plant at Port Kembla as a possible point source of Cu contamination in the Port Kembla region. Copper concentrations in soils from the Boolaroo region were also high and ranged from 2.6 (subsoil) to 223 (topsoil) mg kg 1. The mean Cu concentration in the topsoil and subsoil were 78 and 14 mg kg 1, respectively. Tam and Singh (2004) also reported similar Cu values and a range between 5.1 to mg kg 1 in soils adjacent to the smelter in Boolaroo. Twenty three percent of the 22 samples from this region had Cu concentrations exceeding the EIL (100 mg kg 1 ). These

11 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA 111 findings indicate the smeltering plant at Boolaroo is a possible point source of Cu contamination of soils in the Boolaroo region. All 75 soil samples investigated in the Sydney Basin and Cowra regions were below the EIL (100 mg kg 1 ). The Cu concentrations ranged from between 1.1 and 96.4 mg kg 1, which is within the background range of Australian soils (2 100) (NEPC, 1999) and the worlds soils (2 and 250 mg kg 1 ) (Alloway, 1995). The elevated levels of Cu in the topsoil layer of soils across all regions, particularly in Port Kembla and Boolaroo, suggest anthropogenic sources of Cu contamination. Across all regions, positive linear correlations were observed between soil Cu and CEC (r = 0.565) and organic carbon (r = 0.520), suggesting the binding of soil Cu is greater in organic/mineral soils. As with Cd, this may have resulted in the retention of Cu in the topsoils where higher Cu levels were observed (Figure 2b). Strong correlations were also found with soil Zn (r = 0.726) and soil Cd (r = 0.607) Lead Soil Pb in different regions showed a trend similar to Cd values (Figure 2c). The highest concentrations of soil Pb were found at Boolaroo, ranging between 12 (subsoil) to 1626 (topsoil) mg kg 1. The mean Pb concentrations between layers were significantly different ( P < 0.001), and were 363 (topsoil) and 64 (subsoil) mg kg 1, respectively. Similar levels in the Boolaroo region were reported by Tam and Singh (2004), with Pb levels ranging between 20 to 3609 mg kg 1.However, the results from this study are at the lower end of the range by Galvin et al. (1992), who reported elevated soil Pb levels ranging between mg kg 1 in the suburbs surrounding the smeltering plant in Boolaroo. Three of the 22 soil samples investigated exceeded the 600 mg kg 1 EIL (NEPC, 1999). Background Pb concentrations in Australian soils occurs between 2 and 200 mg kg 1 (NEPC, 1999), and only seven samples exceeded the upper limit. The topsoil Pb concentration at Boolaroo was significantly higher (P < 0.001) than in the topsoils across the remaining regions. Elevated Pb levels were also found at Port Kembla, with values ranging from 13.9 (subsoil) to (topsoil) mg kg 1. The Pb levels in all soils sampled from this region were well below the 600 mg kg 1 EIL. These results corroborate with findings by Beavington (1973), who found elevated Pb levels ( mg kg 1 ) from industrial areas and alongside highways within the Wollongong area. Similarly, Merry and Tiller (1978) also found elevated Pb levels ( mg kg 1 )insoils in the vicinity of a Pb and Zn smelters in Port Pirie, South Australia. The Port Kembla and Boolaroo regions both had significantly higher levels of Pb in the topsoil, as compared to the subsoil and the topsoils from the other two regions; this further suggests anthropogenic pollution associated with the smelting industries in these regions. Sydney Basin had Pb levels ranging between 2.8 (subsoil) to mg kg 1 (topsoil) and Pb in the topsoil (mean = 19.2 mg kg 1 )was generally higher than

12 112 A. G. KACHENKO AND B. SINGH in the subsoil (mean = 13.6 mg kg 1 ). The higher Pb concentrations in the Sydney Basin may be a result of atmospheric deposition from mixed anthropogenic sources including, motor vehicle emissions, sewage sludge additions or through other industrial emissions. The Cowra region had the lowest soil Pb concentrations (Figure 2c), ranging between 7.3 (subsoil) to 11.6 mg kg 1 (topsoil). The Pb concentrations in both the Sydney Basin and Cowra regions were well below the EIL (600 mg kg 1 ). Across all soils, positive linear correlations were observed between soil Pb and organic carbon (r = 0.574) and CEC (r = 0.522), which may account for the elevated concentrations of Pb in topsoils across all regions Zinc Soil Zn concentrations were greatest at the Boolaroo region (Figure 2d), where values occurred between 45 (subsoil) to 4014 mg kg 1 (topsoil). The mean concentrations for topsoils and subsoils were 1062 and 291 mg kg 1 respectively, indicating a significant decrease ( P < 0.001) in Zn concentration with depth. The topsoil concentration of Zn at Boolaroo was significantly different ( P < 0.001) than the topsoil concentrations at the other three regions. The NEPC (1999) EIL of 200 mg kg 1 wasexceeded in 73% of the samples from this region. Tam and Singh (2004) found similar values in the vicinity of the smeltering complex at Boolaroo, which ranged from 20 to 2613 mg kg 1. Elevated levels of Zn were also observed in the Port Kembla region, where values ranged between 86.7 and 1947 mg kg 1, and the topsoil and subsoil mean concentrations were 471 and 282 mg kg 1 respectively. Sixty nine percent of the Port Kembla soils exceeded the EIL (200 mg kg 1 ). Cartwright et al. (1976) found similar levels of Zn in residential sites surrounding a smeltering plant in Port Pirie, South Australia ( mg kg 1 ). The concentration of Zn in soil from the Sydney Basin and Cowra regions were similar (Figure 2d), with only one of the 75 soil samples exceeding the EIL (200 mg kg 1 ). Across both regions values ranged from 8.4 mg kg 1 in the subsoil to mg kg 1 in the topsoil, with a mean of 59.1 mg kg 1. These values were similar to those reported by Jinadasa et al. (1997) for the Greater Sydney Region, who found Zn ranging from 8 to 196 mg kg 1, with a mean of 51 mg kg 1. The range of Zn reported by McKenzie (1960) in Australian soils (11 86 mg kg 1 )was exceeded by 97% of the soils sampled from the Boolaroo and Port Kembla regions combined, compared to only 17% from the Sydney Basin. All Zn values for samples from the Cowra region occur within this range. These results show a significant difference between regional Zn levels (Figure 2d), with higher values in the Boolaroo and Port Kembla regions indicating a significant level of anthropogenic pollution, likely a result of the smelters in the vicinity of the sampling sites. Across all soils significant positive correlations existed between soil Zn and organic carbon (r = 0.544) and CEC (r = 0.726). This suggests the retention of Zn in soils with a high organic matter content and CEC, and may have accounted for higher Zn concentrations in topsoil across the regions.

13 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA Arsenic Soil As was highest in the Boolaroo region (Figure 2e) and the concentrations ranged between 2.5 (subsoil) and 65.0 (topsoil) mg kg 1. The mean topsoil and subsoil concentrations were 14.8 and 10.7 mg kg 1, respectively. Elevated As concentrations were also observed at Port Kembla as the values ranged between <0.01 (subsoil) and 62.5 (topsoil) mg kg 1. The topsoil (mean = 8.8 mg kg 1 ) and subsoil (mean = 6.8 mg kg 1 ) concentrations were similar to those observed for the Boolaroo region. At Boolaroo and Port Kembla, 23 and 38%, respectively of samples exceeded the NEPC (1999) EIL of 20 mg kg 1. The levels from both the Boolaroo and Port Kembla regions (< mg kg 1 ) were considerably lower than those reported by Temple et al. (1977) ( mg kg 1 )inthe vicinity of a secondary Pb smelter in Canada. Background concentrations of As in urban surface soil from non-industrial sites in Australia, range from 0.2 to 45.0 mg kg 1 (Tiller, 1992), and all but 2 samples from these two regions fall within this range. The As concentrations at Boolaroo and Port Kembla were significantly different than those found in the Sydney Basin and Cowra regions (P < 0.001). Two samples from the Sydney Basin had As concentrations exceeding the EIL (20 mg kg 1 ). The remaining soils and all soils sampled from Cowra were below the EIL. All soils sampled from the Sydney Basin were within the Australian background range of soil As defined by Tiller (1992), and all samples from Cowra were below the background range of As concentrations in Australian rural soils (<1 8 mg kg 1 ) (Tiller, 1992) TOTAL ELEMENT ANALYSIS IN PLANTS Plant As levels were omitted as all concentrations were below the detection limit of the ICP-AES (0.1 mg kg 1 ). The remaining metals Cd, Cu, Pb and Zn are expressed on a plant fresh weight basis (FW). Metal concentrations calculated in a dry weight basis (DW) were converted to a FW basis by diluting the metal concentration according to the ratio of FW to DW Cadmium Cadmium concentrations were highest in vegetables at Boolaroo (Table II), with levels ranging from (lettuce) to 2.22 (mint) mg kg 1 FW. The concentration of Cd in vegetables at Boolaroo were significantly higher than those observed at Port Kembla, Sydney Basin and Cowra (P < 0.001). Similar levels were reported by Davies and White (1981) in vegetables grown on soils contaminated by base metal mining in north east Wales and England. The results from Boolaroo indicate that 95% of the vegetables sampled, exceeded the ANZFA 0.1 mg kg 1 FW ML for Cd allowable in vegetable crops. In addition, 68% of samples exceeded the ML for Cd set by the Commission of the European Communities and the Codex Alimentarius Commission (0.2 mg kg 1 FW for leafy vegetables and fresh herbs, 0.1 mg kg 1 for stem and root vegetables). Of the vegetables exceeding the

14 114 A. G. KACHENKO AND B. SINGH TABLE II Geometric mean (±SD), median and range of some important chemical and physical soil properties of the studied soils Cd a Cu a Pb a Zn a Vegetable Range Mean ± SD Range Mean ± SD Range Mean ± SD Range Mean ± SD Cowra Beetroot (n = 2 b ) <0.05 <0.05 ± ± <0.02 <0.02 ± ± Cabbage (n = 2) ± ± <0.02 <0.02 ± ± Lettuce (n = 8) ± ± < (3 c ) ± ± 2.01 Spinach (n = 4) ± < ± < (3) ± ± 1.23 Boolaroo Leek (n = 2) (2 c ) ± ± (2) 2.43 ± ± 2.25 Lettuce (n = 6) (5) ± ± (6) 2.49 ± ± 7.35 Mint (n = 4) (4) 1.89 ± ± (4) 43 ± ± 14.8 Spinach (n = 10) (10) ± ± (10) 4.31 ± ± 31 Sydney Basin Cabbage (n = 6) < ± ± 8.61 < (1) ± ± 4.79 Leek (n = 2) ± ± (2) ± ± 11 Lettuce (n = 36) < (1) ± ± < (12) ± ± 2.69 Parsley (n = 10) ± ± 2.43 < (6) ± ± 5.18 Rhubarb (n = 4) (1) ± ± <0.02 <0.02 ± ± Spinach (n = 24) < (3) ± ± < (4) ± ± 33 Port Kembla Leek (n = 2) ± < ± (2) ± ± 2.01 Lettuce (n = 6) (1) ± ± < (3) ± ± 8.50 Parsley (n = 4) (2) ± ± 1.46 < (3) ± ± 14.5 Spinach (n = 6) ± ± 8.31 < (2) ± ± 9.99 a Values are reported in mg kg 1 FW. b Number of samples. c The number of samples exceeding the Australian Food Standards ML for Cd (0.1 mg kg 1 FW) and Pb (0.3 mg kg 1 FW for brassicas and leafy vegetables, and 0.1 mg kg 1 FW for all remaining vegetables) are indicated in brackets.

15 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA 115 ANZFA guideline value, mint had the greatest concentration of Cd (1.89 mg kg 1 FW) followed by spinach (0.361 mg kg 1 FW), lettuce (0.213 mg kg 1 FW) and leek (0.175 mg kg 1 FW). The high accumulation of Cd in vegetables at Boolaroo may be attributed to the acidic nature of the soil (Table I), resulting in greater Cd availability (Singh et al., 1995), or the adsorption of aerial deposited Cd by vegetable leaves. The Cd values from the remaining three regions were similar, ranging from <0.05 to mg kg 1 FW. In the Sydney Basin, 6% of samples exceeded the ANZFA ML for Cd, with 1% of samples exceeding the ML for Cd set by the Commission of the European Communities and the Codex Alimentarius Commission. Vegetables exceeding the ANZFA guidelines comprised of spinach (3), lettuce (1) and rhubarb (1). Cadmium levels in the present study are higher than those reported by Hardy (2002) in a random market basket survey of Cd levels in vegetables from the Sydney Flemington markets. In that survey, Cd levels did not exceed the ANZFA ML of 0.1 mg kg 1 FW. Conversely, an earlier study by Jinadasa et al. (1997) reported 24% of vegetables sampled from across the greater Sydney Basin exceeded the ANZFA 0.1 mg kg 1 ML for Cd in fresh vegetables. At Port Kembla, 19% of vegetables sampled exceeded the ANZFA ML for Cd. Vegetables exceeding the guidelines included parsley (2) and lettuce (1). In Cowra, all vegetables sampled fell below the ANZFA guideline value for Cd (< mg kg 1 FW) and suggests the relatively pristine nature of this region as compared with Boolaroo, Port Kembla and the Sydney Basin. Across all vegetables sampled, the order of uptake was mint (1.89 mg kg 1 FW) > spinach (0.111 mg kg 1 FW) > leek (0.09 mg kg 1 FW) > rhubarb (0.08 mg kg 1 FW) > lettuce (0.04 mg kg 1 FW) > parsley (0.035 mg kg 1 FW) > cabbage (0.022 mg kg 1 FW) > beetroot (0.005 mg kg 1 FW). Across all vegetables sampled, the concentration of Cd was positively correlated with soil Cd (r = 0.674), soil Zn (r = 0.678) and vegetable Zn concentrations (r = 0.717). These findings suggest interactions between Cd and Zn in both plant and soil are important in determining plant uptake of Cd. Xue and Harrison (1991) identified a synergistic effect of Zn in relation to Cd uptake. They found that increasing the amount of Zn (>600 mg kg 1 )insoils containing high levels of Cd (10 mg kg 1 ), resulted in a higher concentration of Cd in lettuce leaves. Similarly, Smilde et al. (1992) found high concentrations of Cd in leafy vegetables when soil Zn concentrations increased. This synergistic relationship may have resulted in the elevated level of Cd in vegetables sampled from Boolaroo. Moreover, McKenna et al. (1993) identified a strong antagonistic effect of Zn on the accumulation of Cd in leafy vegetables at low Cd concentrations, which may explain the lower concentrations found in vegetables sampled from Cowra, Port Kembla and Sydney Basin Lead Similar to Cd, Boolaroo had the highest concentration of Pb in vegetables sampled (Table II), ranging between (Lettuce) and 57 (mint) mg kg 1 FW. The

16 116 A. G. KACHENKO AND B. SINGH vegetables at Boolaroo had significantly higher concentrations than vegetables sampled at Port Kembla, Sydney Basin and Cowra (P < 0.001). Studies of Pb mobility in leafy vegetables have shown the partitioning of Pb greatest in roots, followed by a decreasing concentration gradient in aboveground biomass (Rahlenbeck et al., 1999; Finster et al., 2004). Hence, the elevated concentrations of Pb in vegetables from Boolaroo may be a result of foliar uptake of aerial Pb deposits originating primarily from the nearby smelter. Of these 22 vegetables, all exceeded the ANZFA ML for Pb allowable in vegetable crops (0.3 mg kg 1 FW for brassicas and 0.1 mg kg 1 FW for all remaining vegetables), and the ML set by the Commission of the European Communities and the Codex Alimentarius Commission (0.3 mg kg 1 FW for brassicas and leafy vegetables, and 0.1 mg kg 1 FW for all remaining vegetables). Mint had the greatest concentration of Pb ( mg kg 1 FW) followed by spinach ( mg kg 1 FW). Of the remaining vegetables, the mean concentration of Pb was 2.49 mg kg 1 FW for lettuce and 2.43 mg kg 1 FW for leek. Lead levels in vegetables across the regions of Cowra, Port Kembla and the Sydney Basin were similar (Table II). Levels observed in the Sydney Basin were generally low, the order of uptake: parsley > leek > lettuce > cabbage > spinach > rhubarb. Of these samples, 32% exceeded the ANZFA ML for Pb allowable in vegetable crops, whereas 16% exceeded the ML set by the Commission of the European Communities and the Codex Alimentarius Commission. Vegetables exceeding the ANZFA guidelines comprised of lettuce (12), parsley (6), leek (1), spinach (4) and cabbage (1). The locations of these sites were in built up areas and generally in the close vicinity of major roadways, which may have contributed to these elevated levels. Lead levels at Port Kembla ranged from <0.02 to mg kg 1 FW, with 60.1% of these samples exceeding the ANZFA ML for Pb. Thirty three percent of these samples exceeded the MLs set by the Commission of the European Communities and the Codex Alimentarius Commission. Of the vegetables exceeding the ANZFA guidelines, leek had the greatest mean concentration (0.484 mg kg 1 FW) followed by parsley (0.256 mg kg 1 FW), spinach (0.125 mg kg 1 FW) and lettuce (0.176 mg kg 1 FW). The higher levels observed in these vegetables may be attributed to the smelter located in the nearby vicinity of the sampling sites, indicating uptake from aerial sources. Thirty eight percent of samples from Cowra exceeded the ANZFA ML for Pb, whereas only 19% exceeded the ML for Pb set by the Commission of the European Communities and the Codex Alimentarius Commission. Levels ranged between < mg kg 1 FW. Vegetables that exceeded the ANZFA guidelines were lettuce (3) and spinach (3). Sources of Pb in vegetables sampled from the Cowra region may have occurred from impurities in pesticides, fertilisers, sewage sludge or manure. Vegetables consumed as part of a balanced diet may contribute to increased blood Pb levels with increased risk of anaemia and neurological disorders (Gupta

17 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA 117 and Gupta, 1998; Hunter Health, 2003). In Australia, the National Health and Medical Research Council (NHMRC) advise that blood Pb levels should be no more that 10 micrograms per decilitre (µg/dl) (NHMRC, 1993). In the suburbs directly surrounding the smelter at Boolaroo, blood Pb testing has been offered to the public, particularly children who are more susceptible to Pb toxicity. In the year July 2002 June 2003, 31% of 200 children under the age of 13 and 37% of 94 children under the age of 5 had blood Pb levels greater or equal to 10 µg/dl (Hunter Health, 2003). In Port Kembla, a study by Kreis et al. (1994) reported fewer cases of children exceeding the NHMRC suggested guideline of blood Pb (10 µg/dl). Of 182 children between the ages of 1 4, close to 11% had blood Pb levels greater or equal to 10 µg/dl. In children between the ages of 1 6, more than 9% exceeded the guideline value. The study also identified a group of children with elevated blood Pb levels living within a 1 km radius of the Cu smelter. These studies suggest that the smelters located in both regions are important sources of Pb pollution which can affect human health and furthermore, reflects the greater Pb concentrations in vegetables found in Boolaroo than those sampled in Port Kembla Zinc The levels of Zn in vegetables showed a similar trend to Cd and Pb levels (Table II). The vegetables sampled at Boolaroo were significantly higher ( P < 0.001) than levels found at Port Kembla, Sydney Basin and Cowra. Vegetables sampled at Boolaroo ranged between 7.70 (leek) 159 (mint) mg kg 1 FW. Of the vegetables sampled in Boolaroo, the order of Zn uptake was: mint (146 mg kg 1 FW) > spinach (54 mg kg 1 FW) > lettuce (12.9 mg kg 1 FW) > leek (9.28 mg kg 1 FW). Dowdy and Larson (1975) showed plant Zn is highly dependent on its concentration in soils and furthermore reported a higher uptake of Zn in leafy vegetables. In vegetables sampled from Boolaroo, the elevated soil Zn concentrations (Figure 1) may have resulted in greater uptake and accumulation of Zn. Furthermore, foliar adsorption of Zn as a result of smelter emissions may have also contributed to an increase in Zn concentrations in vegetables sampled. The Zn concentrations in vegetables from the Sydney Basin and Port Kembla regions were similar (Table II). The Zn levels in the Sydney Basin ranged from 1.47 (lettuce) to 128 (spinach) mg kg 1 FW, and at Port Kembla ranged between 1.97 (lettuce) and 25 (spinach) mg kg 1 FW. From vegetables sampled in both regions, the order of uptake was: parsley (19.92 mg kg 1 FW) > spinach (18.7 mg kg 1 FW) > leek (17.5 mg kg 1 FW) > rhubarb (13.7 mg kg 1 FW) > cabbage (8.13 mg kg 1 FW) > lettuce (5.31 mg kg 1 FW). Both regions are influenced by anthropogenic contamination which may have resulted in some higher concentrations in vegetables sampled. Zinc concentrations in the Cowra region were consistently lower than vegetables sampled across all regions, ranging from 1.50 (lettuce) 6.73 (lettuce) mg kg 1 FW. The levels of Zn in the vegetable crops at this region are similar to those found in vegetable crops surveyed across commercial

18 118 A. G. KACHENKO AND B. SINGH areas of the United States of America (Shacklette, 1980). At present there are no international guidelines stipulating the maximum levels of Zn permissible in food products. The concentration of Zn in the vegetables sampled across all regions was strongly correlated with soil Zn content (r = 0.610), plant Cd (r = 0.717) and soil Cd (r = 0.567). The relationship between Cd Zn has been addressed in detail in Section Copper Copper concentrations in vegetables were highest at Port Kembla (Table II), and ranged from to 19.3 mg kg 1 FW. Spinach accumulated the greatest concentration of Cu (6.87 mg kg 1 FW) followed by leek (3.24 mg kg 1 FW), parsley (2.27 mg kg 1 FW) and lettuce (1.96 mg kg 1 FW). The concentration of Cu in vegetables sampled at Port Kembla were significantly higher ( P < 0.001) than concentrations found at Boolaroo, Cowra and the Sydney Basin, which suggests the smelter may be an important source of Cu contamination. An earlier study by Beavington (1975) of vegetables grown in residential gardens around the Port Kembla smelter observed concentrations of Cu in lettuce that were twice that of those sampled in this study. Levels of Cu in vegetables across the remaining regions were similar (Table II). At Boolaroo the concentrations ranged from (lettuce) to 7.03 (mint) mg kg 1 FW, in the Sydney Basin they ranged from (lettuce) to 23 (cabbage) mg kg 1 FW and in Cowra they ranged from (lettuce) to 1.04 (beetroot) mg kg 1 FW. Preer et al. (1980) reported similar levels of Cu in vegetables from urban gardens in the city of Washington D.C, USA and similar concentrations were also observed in vegetables grown near an industrial area in Greece (Vousta et al. 1996). Some vegetables sampled from the Sydney Basin showed higher Cu concentrations which may be a result of foliar absorption of Cu through the use of Cu laden fungicide sprays commonly used on commercial vegetable farms. Similar to Zn, there are no international guidelines to enforce the ML of Cu in vegetable crops SOIL-PLANT TRANSFER COEFFICIENTS The transfer coefficient quantifies the relative differences in bioavailability of metals to plants and is a function of both soil and plant properties. The coefficient was calculated by dividing the concentration of a metal in a vegetable crop (DW) by the total metal concentration in the soil. Higher transfer coefficients reflect relatively poor retention in soils or greater efficiency of plants to absorb metals. Low coefficients reflect the strong sorption of metals to the soil colloids (Alloway and Ayres, 1997). Table III outlines the range of transfer coefficients (Cd, Cu, Pb and Zn) calculated for each region. The table also contains a range of generalized transfer coefficients, which have been suggested by Kloke et al. (1984). Kloke s transfer

19 HEAVY METALS CONTAMINATION OF VEGETABLES IN AUSTRALIA 119 TABLE III The range of transfer coefficients of metals and their suggested coefficient range Range Heavy Cowra Boolaroo Sydney Basin Port Kembla Suggested metal (n = 16) (n = 22) (n = 82) (n = 18) range a Cd (2 b ) Cu (18) (73) (10) Pb < (6) (14) < (14) < Zn < (2) a Kloke et al. (1984). b The value in brackets indicates the number of samples exceeding the suggested range of generalised transfer coefficients. coefficients are based on the root uptake of metals, with no consideration given to aerial deposition and foliar adsorption of elements. Most of the soil-plant transfer coefficients from the Cowra region were below the suggested range (Table III) reported by Kloke et al. (1984). Only six leafy vegetables (3 lettuce samples and 3 spinach samples) exceeded the suggested coefficient range for Pb. In the remaining three regions, our results show the suggested coefficient range is commonly exceeded for Pb and Cu. Vegetables identified with high mean Cu transfer coefficients included leek (0.90), spinach (0.64) and lettuce (0.46). For Pb, high transfer coefficients were identified in cabbage (1.38), lettuce (0.84) and mint (0.30). At Boolaroo, it was suspected that high Pb and Cu transfer coefficients were a combined result of elevated topsoil metal concentrations (363 mg kg 1 for Pb and 223 mg kg 1 for Cu) and adsorption of atmospheric metal deposits in vegetables from the nearby smelter. Tiller et al. (1987) reported that soil could be contaminated with heavy metals by aerial deposition for up to hundreds of kilometres away from the source. At Port Kembla, high concentrations of Cu in the topsoil (mean = 1032 mg kg 1 ) are likely to have resulted in greater vegetable uptake. Aerial metal deposits may have further contributed to vegetable Cu concentrations resulting in elevated transfer coefficients. These results suggest that there is a high soil-plant transfer of Cu and Pb to leafy vegetables in regions where there was evidence of anthropogenic metal contamination. In the Sydney Basin, foliar application of Cu through the application of fungicide sprays (particularly commercial sites) may have resulted in the high number of samples exceeding the suggested coefficient range for Cu. Soil properties may have further influenced the soil-plant transfer of Cu and Pb. The slightly acidic nature of the topsoils from Boolaroo (mean ph of 6.49), Port Kembla (mean ph of 6.65) and the Sydney Basin (mean topsoil ph of 6.22) may have increased the availability of metals for vegetable uptake. Furthermore, the