Accumulation of heavy metals in leaf vegetables from agricultural soils and associated potential health risks in the Pearl River Delta, South China

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1 Environ Monit Assess (2014) 186: DOI /s Accumultion of hevy metls in lef vegetbles from griculturl soils nd ssocited potentil helth risks in the Perl River Delt, South Chin C. Y. Chng & H. Y. Yu & J. J. Chen & F. B. Li & H. H. Zhng & C. P. Liu Received: 9 My 2013 /Accepted: 1 October 2013 /Published online: 3 November 2013 # The Author(s) This rticle is published with open ccess t Springerlink.com Abstrct This study investigted the extent of hevy metl ccumultion in lef vegetbles nd ssocited potentil helth risks in griculturl res of the Perl River Delt (PRD), South Chin. Totl concentrtions of mercury (Hg), cdmium (Cd), led (Pb), chromium (Cr) nd rsenic (As) were determined in 92 pirs of soil nd lef vegetble (flowering Chinese cbbge, lettuce, pkchoi, Chinese cbbge, loose-lef lettuce, nd Chinese lef mustrd) smples collected from seven griculturl res (cities). The bioconcentrtion fctors (BCF) of hevy metls from soil to vegetbles were estimted, nd the potentil helth risks of hevy metl exposure to the PRD residents through consumption of locl lef vegetbles were ssessed. Results showed tht mong the six lef vegetbles, pkchoi hd the lowest cpcity for hevy metl enrichment, wheres mong the five hevy metls, Cd hd the highest cpcity for trnsferring from soil into vegetbles, with BCF vlues 30-fold those of Hg C. Y. Chng Gungzhou Institute of Geochemistry, Chinese Acdemy of Sciences, Gungzhou , Chin C. Y. Chng : H. Y. Yu : J. J. Chen : F. B. Li (*) : H. H. Zhng : C. P. Liu Gungdong Public Lbortory of Environmentl Science nd Technology, Gungdong Institute of Eco-Environmentl nd Soil Sciences, Gungzhou , Chin e-mil: cefbli@soil.gd.cn C. Y. Chng Grdute University of Chinese Acdemy of Sciences, Beijing , Chin nd 50-fold those of Cr, Pb nd As. Sewge irrigtion nd fertiliztion were likely the min sources of hevy metls ccumulted in lef vegetbles grown in griculturl res of the PRD region. Different from previous findings, soil ph hd no cler effect on metl ccumultion in lef vegetbles. Despite certin degree of metl enrichment from soil to lef vegetbles, the PRD residents were not exposed to significnt helth risks ssocited with consumption of locl lef vegetbles. Nevertheless, more ttention should be pid to children due to their sensitivity to metl pollutnts. Keywords Perl River Delt. Lef vegetbles. Hevy metls. Bioconcentrtion fctor. Trget hzrd quotient Introduction Hevy metls cn ccumulte nd migrte in soil environments. Due to their cumultive effects nd long-term interctions, ccumultion of hevy metls in soil negtively ffects regionl eco-sfety nd poses thret to relevnt nimls nd plnts. Additionlly, hevy metls cn enter humn bodies through the food chin, leding to n incresed incidence of chronic diseses such s deformity nd cncer (Müller nd Anke 1994; Rmdn nd Al-Ashkr 2007; Tembo et l. 2006). Studies hve shown tht fruit nd vegetble consumption is the primry pthwy of humn exposure to hevy metls (Adms et l. 2004; McLughlin et l. 1999). Therefore, it is of prcticl significnce to ssess the extent of hevy metl ccumultion from soil into plnts such s fruits nd

2 1548 Environ Monit Assess (2014) 186: vegetbles, nd relevnt reserch hs gined incresing ttentions. The behviors of metl in soils re very complex, which involve dsorption desorption, complextion dissocition, oxidtion reduction, ion exchnge, nd other crrier trnsport role. The former two rections minly ffect metl ctivity in soil, while oxidtion reduction cn lso chnge metl vlence (Swrtjes et l. 2007). These chemicl mechnisms cn work together nd ffect one nother, which formed complex interction system controlling metl ftes. Hevy metls enter the vegetble tissues minly through the roots nd folige, of which root uptke ws the dominnt pthwy. Metls cn be trnsferred from soil pore wter into the plnts though the roots in the form of dissolved ions (e.g., Cd 2+ ) (McLughlin et l. 2011). Series of complex processes occur in the soil pore wter nd crop rhizosphere. The degree of metl enrichment in crops cn be described with enrichment fctor, which is defined s the rtio of prticulr element content in plnt to tht in soil. The concept of enrichment fctor ws first proposed by Zoller et l. (1974) for source dignosis of tmospheric prticulte mtter in the Antrctic. In the following yer, enrichment fctor ws used for investigting high-ltitude tmospheric substnces in the North Atlntic Ocen (Duce et l. 1975). Recently, the ppliction of enrichment fctor in the form of trnsfer fctor, bioconcentrtion fctor (BCF), nd plnt uptke fctor hs been expnded to reserch on soil, wter system, nd sediment, s well s ssessment of hevy metl pollution in environmentl geochemistry (Wng et l. 2006, b; Khn et l. 2010; Brioschi et l. 2013; Delgdo et l. 2012). In soil reserch, BCF is defined s the rtio of the content of prticulr element in plnt to tht in soil. BCF is n importnt quntittive indictor of crop contmintion nd hs commonly been used for estimting metl trnsfer from soil into plnts (Grcí et l. 2009; Melgr et l. 2009; USEPA 2005). BCF-bsed reserch shows tht the extent of metl enrichment in vegetbles is highest in lef vegetbles, followed by tubers nd fruit vegetbles (Liu et l. 2012; Pndey nd Pndey 2009). Regrding metl concentrtions, cdmium (Cd) nd led (Pb) commonly occur t high levels in lef vegetbles while the Zn content of tubers is higher thn other metl contents (Ngole 2011). The biovilbility nd toxicity of metls in soil re significntly influenced by ph condition (Bdwy et l. 2002;Wng et l.2006b). Soil ph is considered to be one of the most importnt fctors tht influence the trnsfer of CdndPbfromsoiltoplnts,ndhigherpHvlueshve been found to reduce the biovilbility nd toxicity of Cd nd Pb (McBride et l. 1997;Gryetl.1999). There re mny reserchers who devote themselves to the reserch on the reltion between soil ph nd Cd uptke (Cost nd Morel 1993; Hrt etl. 2002; Kim et l. 2002; Tudoren nd Phillips 2004; McLughlin et l. 2011). The consistent conclusion is tht the dsorption between soil prticles nd Cd increses with the increse of soil ph, while Cd biovilbility decresed. The mechnism for this phenomenon cn contribute to the increses of solubility nd ion competition. As the soil ph decreses, the concentrtions of Fe 2+,Mn 2+,Zn 2+,ndC 2+ increse in soil solution, which enhnce the competition of free ions nd reduce the dsorption to soil prticles (Tudoren nd Phillips 2004). Additionlly, Speir et l. (2003) reported tht soil ph is the gretest determinnt of the solubility nd mobility of chromium (Cr), Pb nd Zn in sndy soil. Due to the close reltion between soil ph nd hevy metl properties, correltion nlysis of ph vlue nd hevy metl ccumultion is commonly ppliedinreserchonccumultionofhevymetlfrom soil to vegetbles. The Perl River Delt (PRD) region in South Chin covers n re of 54,733 km 2, with 13,357 km 2 of griculturl lnd nd 4,829 km 2 of vegetble re (Fig. 1) (Gungdong Sttistics Bureu 2012; Lu 1988). The PRD region is the lrgest vegetble production bse in Gungdong Province nd produced 11,291,987 tons of vegetble in It minly exports to Hong Kong nd Mco, which receive more thn 50 % of the totl export volume of vegetbles from the PRD (Gungdong Sttistics Bureu 2012). Being one of the most developed regions in Chin, the PRD region hs experienced substntil industril pollution in recent decdes. Associted soil nd ir pollution cn enhnce pollutnt ccumultion in vegetbles, further incresing potentil humn helth risks. However, previous studies on hevy metl ccumultion in soil nd/or vegetble in the PRD region were minly focused on polluted soils in suburb, industril or mining res. Presently, there is lck of report on hevy metl uptke by vegetbles in lrge griculturl bses in the PRD region (Luo et l. 2011;Zhoetl.2012). To this end, the present study ssessed the extent of hevy metl ccumultion in lef vegetbles commonly grown in griculturl res in the PRD region. Totl concentrtions of mercury (Hg), Cd, Pb, Cr nd rsenic (As) were determined in 92 pirs of lef vegetble nd soil smples. The ccumultion of hevy metls in lef

3 Environ Monit Assess (2014) 186: vegetbles ws interpreted using BCF, nd the reltion between BCF vlues nd soil ph ws exmined by principl component nlysis (PCA) nd Person correltion nlysis. The potentil humn helth risks of hevy metl exposure to the PRD residents through consumption of locl lef vegetbles were evluted using the trget hzrd quotient (THQ). The results will provide reference dt for further investigtion of hevy metl ccumultion in the PRD region, thereby improving the regionl food sfety. Mterils nd methods Soil nd vegetble smpling nd processing Ninety-two pirs of soil nd vegetble smples were collected in the PRD region during September November 2011 (Fig. 1). The smpling loctions were chosen from lrge vegetble bses nd ntionl bsic frmlnd protection zones (>30 h) distnt from urbn nd industril res. Six kinds of lef vegetbles were collected during the hrvest period, including flowering Chinese cbbge (Brssic cmpestris L. ssp. chinensis vr. utilis Tsen et Lee), lettuce (Lctuc stiv L. vr. romn Hort), pkchoi (Brssic chinensis L.), Chinese cbbge (Brssic pekinensis (Lour.) Rupr), loose-lef lettuce (Lctuc stiv L.), nd Chinese lef mustrd (Brssic junce Coss). Soil smples were tken from the surfce lyer (0 20 cm) using bmboo shovel nd gently shken off from the vegetbles roots. All smples were seled in polyethylene bgs nd trnsported to the lbortory within6hofcollection. The soil smples were ir-dried t room temperture, with impurities mnully removed. Then, the soils were ground nd sieved through 80 meshes (0.2 mm). For vegetble smples, the decy nd withered tissues were removed nd the edible prts were wshed with tp wter to remove surfce dirt. The edible prts of vegetbles were repetedly rinsed with deionized wter nd dried t 60 C to constnt weight. The dry vegetble smples were crushed with wooden hmmer in crnelin mortr nd then pssed through n 80-mesh sieve. Hevy metl nd soil ph nlyses The concentrtions of hevy metls in soil nd vegetble smples were determined ccording to the methods of Rsmussen et l. (1991). Briefly, 600 mg of ir-dried soil ws mixed with 6 ml of concentrted HNO 3 HClO 4 (87:13, v/v) nd 6 ml of concentrted HCl. The mixture ws digested nd then dissolved in 2 % HCl solution. The vegetble smples were digested in mixture of HNO 3 HClO 4 H 2 O 2 (87:13:10, v/v/v). The Hg nd As concentrtions of digestion solutions were determined using n tomic fluorescence morphologicl nlyzer (SA-10, Titn, Beijing, Chin), Pb nd Cr concentrtions were determined using WFX-130 flme tomic dsorption spectrophotometer (Bric, Chin), nd the Cd content ws determined using Z-2700 grphite furnce tomic bsorption spectrophotometer (Hitchi, Jpn). Stndrd reference mterils of soil smples (GBW nd GBW07429 (GSS-15)) nd citrus leves (GBW10020 (GSB-11)) were ssyed during smple nlysis for qulity control. Regent blnks were included to ensure detection precision (<5 %). Soil ph ws mesured in soil slurries using 1:2.5 soil-to-wter rtio with PHS-3C ph meter (Srtorius, Chin). Dt nlyses BCF clcultion BCF ws clculted s follows: BCF ¼ C vegetble ð1þ C soil where C vegetble is the totl concentrtion of prticulr hevy metl in the vegetble (mg kg 1 dw), nd C soil is the corresponding hevy metl concentrtion in the soil hbitt of the vegetble (mg kg 1 ). Vegetble consumption-ssocited helth risk ssessment Potentil helth risks of hevy metl exposure to PRD residents through locl lef vegetble consumption were ssessed using THQ tht ws first proposed by the United Sttes Environmentl Protection Agency (USEPA) for ssessing the potentil helth risks of pollutnt exposure to humn helth (USEPA 2002; Liu et l. 2006; Song et l. 2009; Wng et l. 2005). THQ is defined s the rtio of the body intke dose of pollutnt to the reference dose (Eqs. 1 nd 2). If THQ> 1, there will be potentil risk ssocited with this

4 1550 Environ Monit Assess (2014) 186: Fig. 1 Agriculturl soil nd lef vegetble smplings loctions in the Perl River Delt region, South Chin (plus sign, flowering Chinese cbbge; dimond, lettuce; blck circle, pkchoi; tringle, Chinese cbbge; white str, loose-lef lettuce; blck str, Chinese lef mustrd) PRD pollutnt. If THQ<1, there will be no obvious potentil risk ssocited with this pollutnt. Single pollutnt : THQ ¼ C IRvegetble EF ED BW AT RfD 10 3 ð2þ Totl pollutnts : Gungdong Province Chin THQtotl ¼ X THQðsingle pollutntþ ð3þ where C is the men concentrtion of prticulr metl in vegetble, IR is the dily vegetble intke by the PRD residents (including locl nd extrneous vegetbles), EF is the exposure frequency (exposure dys per yer), ED is the exposure durtion, BW is the verge weight of locl residents, AT is the verge exposure time for non-crcinogens (exposure dys within whole lifetime), nd RfD is the reference dose. It must be noted tht the present study concerns metl helth risks due to the consumption of locl lef vegetbles. Thus, prmeters of fv (locl vegetbles/totl vegetbles consumption), f (lef vegetble/locl vegetble), nd fb (fruit vegetble/locl vegetble) were introduced in the estimtes of dily locl lef vegetble intke. Sttisticl nlyses Sttisticl nlyses were performed with the SPSS 13.0 softwre pckge. Chrts nd grphs were produced using Origin 8.1. The mp of regionl soil nd vegetble smpling loctions (Fig. 1) ws constructed in ArcGis The reltion between BCF vlues of hevy metls in vegetbles nd ssocited soil ph ws exmined by Person correltion with the levels of significnce t P< 0.05 nd P<0.01 (two-tiled) s well s PCA. Results nd discussion Hevy metl distribution in griculturl soils nd lef vegetbles in the PRD region Totl concentrtions of Hg, Cd, Pb, Cr, nd As in griculturl soils showed lrge vritions in the PRD region (Tble 1). In prticulr, the rnges of Pb, Cr, nd As concentrtions were , , nd mg kg 1, respectively. The verge Hg, Cd, Pb, nd As concentrtions of soil smples were higher thn the bckground metl levels in Gungdong (Soil Survey Office of Gungdong Province 1993), wheres

5 Environ Monit Assess (2014) 186: Tble 1 Concentrtion (mg kg 1 dw, men ± stndrd devition) of hevy metls in soils nd vegetbles in the Perl River Delt region, South Chin Smple type Index Smple number Hg Cd Pb Cr As Soil Men ± SD ± ± ± ± ±20.8 Rnge Bckground level of Gungdong Chinese stndrd for griculturl soil b Vegetble (men ± SD) Flowering Chinese cbbge ± ± ± ± ±0.039 Lettuce ± ± ± ± ±0.034 Pkchoi ± ± ± ± ±0.067 Chinese cbbge ± ± ± ± ±0061 Loose-lef lettuce ± ± ± ± ±0.058 Chinese lef mustrd ± ± ± ± ±0.023 Metl bckground vlue in the soil of Gungdong province (Soil Survey Office of Gungdong Province 1993) b Environmentl Qulity Stndrds for soil (GB , Ntionl Environmentl Protection Agency of Chin) soil Cr concentrtion hd no significnt increses compred to the bckground Cr level in Gungdong (Tble 1). Compred with the vlues in the Environmentl Qulity Stndrds for soil (GB , Ntionl Environmentl Protection Agency of Chin), the men soil Pb nd Cr concentrtions did not exceed the limits. Although the men soil Hg, Cd, nd As concentrtions were below the ntionl stndrd limits (Tble 1), few smples were modertely enriched with one or more thn one of these hevy metls (19/92 for Hg, 11/92 for Cd, nd 10/92 for As). Overll, these results suggest tht Hg, Cd, Pb, nd As were ccumulted in griculturl soils in the PRD region. Regrding regionl distribution, Foshn nd Zhongshn hd reltively higher Cd, Pb, nd Cr concentrtions thn other smpling res (cities) in the PRD region (Fig. 2). Among the seven cities, Jingmen nd Foshn hd the highest verge soil Hg concentrtion, wheres Huizhou hd the highest verge soil As concentrtion. The metl (Hg, Cd, nd As) in some smples exceed the limit vlues recommended by the Environmentl Qulity Stndrds for soil (GB , Ntionl Environmentl Protection Agency of Chin), while no smples contined Pb nd Cr exceeding their limit vlues, respectively. The soil smples with excessive metls (Hg, Cd, nd As) minly cme from Gungzhou (7/32), Zhongshn (4/8), nd Huizhou (9/13), suggesting tht more ttention should be pid to Hg, Cd, nd As pollution in Gungzhou, Zhongshn nd Huizhou, respectively. As compred to the soils, lef vegetbles contined less hevy metl contents with obvious vritions mong different species (Tble 1). The rnges of vegetble Pb concentrtion were mg kg 1 (flowering Chinese cbbge), mg kg 1 (lettuce), mg kg 1 (pkchoi), mg kg 1 (Chinese cbbge), mg kg 1 (loose-lef lettuce), nd mg kg 1 (Chinese lef mustrd), respectively. Of the 92 vegetble smples, there were 10 smples (11 %) contining excessive levels of Pb concentrtion (0.3 mg kg 1 ) nd 27 smples (30 %) contining excessive levels of As (0.05 mg kg 1 ) referred to the Codex Alimentrius Commission (CAC) stndrd vlues. In contrst, the Hg, Cd nd Cr concentrtions of ll vegetble smples were below the CAC (FAO/WHO 2001) stndrd vlues (0.01, 0.2, nd 0.5 mg kg 1, respectively). These results demonstrte tht Pb nd As re the dominnt metl pollutnts ccumulted in lef vegetbles grown in griculturl soils in the PRD region.

6 1552 Environ Monit Assess (2014) 186: Metl concentrtions in soils (mg/kg) Hg*100 Cd*100 Pb Cr As Metls Metl concentrtions in vegetbls (mg/kg dw) 0.5 b Hg Cd Pb Metls Cr As Gungzhou Zhuhi Foshn Jingmen Donggun Zhongshn Huizhou Fig. 2 Metl concentrtions in soils () nd vegetbles (b) from different griculturl res of the Perl River Delt region, South Chin. The numbers of smples in Gungzhou, Zhuhi, Foshn, Jingmen, Donggun, Zhongshn nd Huizhou were 32, 5, 5, 10, 19, 8, nd 13, respectively Regrding regionl distribution, the five metls ccumulted in lefy vegetbles showed different trends from those in soils. The vegetble smples with excessive levels of hevy metls (10/92 for Pb nd 27/92 for As) were minly from Gungzhou (5/32 for Pb nd 5/32 for As) nd Donggun (5/19 for Pb nd 8/19 for As) (Fig. 2b), possibly due to the high degree of industriliztion nd reltively high pollutnt concentrtions in the tmosphere in these two cities (Wong et l. 2003). No vegetbles with excessive levels of hevy metls were found in Foshn or Huizhou. Bioccumultion of hevy metls from soil to vegetbles The BCF vlues of Hg in vegetbles rnged from to nd verged 0.010, nd those of Pb, Cr nd As in vegetbles vried in similr rnges, i.e., , , nd , respectively. By comprison, the BCF vlues of Cd in vegetbles were significntly higher, vrying from to 3.10 nd verging The BCF vlues of Cd were pproximtely 30-fold those of Hg nd 50-fold those of Cr, Pb nd As (Fig. 3). Since greter BCF vlue indictes higher ccumultion potentil of metls in vegetbles (Chumbley nd Unwin 1982; Cui et l. 2004), the bove results indicte tht Cd hs higher cpcity for trnsferring from soil to the edible prts of vegetbles thn the other four hevy metls in griculturl soil of the PRD region. This cn be ttributed to the competition between Cd 2+ nd C 2+.ItisesierforC 2+ to be replced by Cd 2+ thn other metls becuse of their sme ionic rdius nd vlence (Kim et l. 2002; Hrt et l. 2002). In ddition, C is n essentil element for crops nd it cn enter plnt tissues by ctive trnsport, while most hevy metls (s nonessentil elements) cn only enter plnt tissues through pssive methods (e.g., concentrtion diffusion nd permetion) (Cost nd BCF 1.2 Flowering Chinese Cbbge 0.9 Lettuce Pkchoi Chinese cbbge 0.6 Loose-lef lettuce 0.3 Chinese lef mustrd b b b b b b b b b b Hg Pb Cr As Cd Metls Fig. 3 Bioconcentrtion fctor (BCF) vlues of five hevy metls in six kinds of lef vegetbles collected from griculturl soils in the Perl River Delt region, South Chin. Averge vlue within the sme tretment tht hs different lowercse letters (i.e., or b) is significntly different t P<0.05, wheres verge vlue within the sme tretment tht hs the sme lowercse letters is not significntly different t P=0.05

7 Environ Monit Assess (2014) 186: Tble 2 The bioconcentrtion fctor vlues of vegetbles in previous studies Country Smplings site description Hg Cd Pb Cr As References Spin Slopes of hill Men ± SD 0.103±0.011 Millán et l. (2006) Ner mine Men ± SD 0.036±0.003 Ner former mine Men Álvrez-Ayuso et l. (2012) Pkistn Agriculturl lnd Rnge Khn et l. (2010) Wstewter-irrigted soil Men Jn et l. (2010) Chin Vegetble yrds Rnge Wng et l. (2004) Agriculturl soil Rnge Ci et l. (2012) The min crop production sources Rnge Zhng et l. (2011) Vegetble soil Rnge This study Morel 1993). Differently, Cd cn lso enter plnt tissues through C chnnels (Tester 1990). Although there ws no significnt difference between different kinds of vegetbles for most hevy metls, the BCF vlues of different hevy metls showed lrge vritions in the six kinds of vegetble (Fig. 3). In prticulr, flowering Chinese cbbge hd higher BCF verge vlue of Cd (0.521) nd lower vlues of Hg (0.010), Pb (0.004), Cr (0.004), nd As (0.007) thn other kinds of vegetbles. Compred with flowering Chinese cbbge nd lettuce, Chinese cbbge, loose-lef lettuce nd Chinese lef mustrd hd lower BCF verge vlues of Cd nd higher vlues of Hg, Pb, Cr nd As. Among the six lef vegetbles, pkchoi hd the lowest verge BCF vlues of hevy metls (except for As). Thus, there is reltively low potentil for metl ccumultion in pkchoi in the PRD region. The obtined BCF vlues were compred with previously published dt of hevy metl ccumultion in vegetbles from soils ssocited with griculturl lnd use, wstewter irrigtion, nd mining ctivity (Tble 2). Despite showing gret vribility, the BCF vlues of hevy metls in vegetbles from soils impcted by mining, hillslope lndform, or wstewter irrigtion were obviously higher thn those obtined in the present study. This suggests tht there is reltively low potentil for hevy metl ccumultion in griculturl soils in the PRD region, possibly due to their distnt loctions from urbn centers nd industril res. Lef vegetbles generlly grow fster with higher trnspirtion rtes thn non-lef vegetbles (Luo et l. 2011). Thus, metl uptke by plnt roots cn be enhnced in lef vegetbles, resulting in the trnsloction of metls from roots to other vegetble tissues (Stliks Tble 3 Mtrix of principl component nlysis of the bioconcentrtion fctor vlues of hevy metls in vegetbles PC1 PC2 PC3 Hg Cd Pb Cr As Eigenvlue Vrition (%) Cumultive vrition (%)

8 1554 Environ Monit Assess (2014) 186: Tble 4 Coefficients of correltions between soil ph nd bioconcentrtion fctor vlues Flowering Chinese cbbge Lettuce Pkchoi Chinese cbbge Loose-lef lettuce Chinese lef mustrd Smple number Hg Cd Pb Cr As b Correltion is significnt t the 0.05 level (two-tiled) b Correltion is significnt t the 0.01 level (two-tiled) et l. 1997; Zheng et l. 2007). Due to the brod lef re, lef vegetbles re more susceptible to pollutnt ccumultion by the dust from soil nd rinwter. To llevite metl pollution in locl vegetbles, it is suggested to plnt lef vegetbles in soil with low metl content nd non-lef vegetbles in soil with reltively high metl content in lrge griculturl res (Kuchrski et l. 1994; Luo et l. 2011). According to results of the present study, pkchoi cn be plnted with priority in Cdenriched zones, followed by loose-lef lettuce, Chinese cbbge, Chinese lef mustrd, lettuce nd flowering Chinese cbbge. However, metl ccumultion in vegetble tissues cn be strongly influenced by multiple fctors, including soil properties (e.g., soil ph, orgnic mtter, cly content nd metl concentrtion), plnt fctors (e.g., plnt type nd pnting mode), nd other environmentl conditions (e.g., tmosphere nd industril pollution) (Twining et l. 2004). Therefore, cution must be tken when mking specific griculturl plnting plns. Identifiction of hevy metl sources PCA hs commonly been used for investigting metl sources, nthropogenic ctivities, or soil prent mterils (Fcchinelli et l. 2001; Losk nd Wiechuł 2003; Borůvk et l. 2005; Ci et l. 2012). In the present study, three principl components (PC) were extrcted from the BCF vlues of hevy metls in lef vegetbles (Tble 3). The first principl component (PC1) explins 33.0 % of the totl vrince nd loded hevily on Hg (0.833) nd As (0.839). Studies hve shown tht verge Hg concentrtion in wstewterirrigted res is pproximtely 6.9-fold the concentrtion of non-wstewter-irrigted re nd tht Hg contmintion is serious in wstewter-irrigted griculturl soils in the PRD region (Zhu et l. 2005; Chenetl. 2005). Additionlly, study of Hg emission in Gungdong hs shown tht tmospheric Hg fluxes hve no strong correltion with soil Hg concentrtion (Fu et l. 2012). Bsed on the bove findings, we speculte tht PC1 reflects the impcts of sewge irrigtion. The second principl component (PC2) ccounts for 25.1 % of the totl vrince nd is dominted by Cd (0.593), Pb (0.587), nd Cr (0.727). Becuse the men soil Cr concentrtion (46.7 mg kg 1 ) ws lower thn the bckground level in Gungdong (56.5 mg kg 1 ), the Cr ccumulted in vegetbles could minly come from nturl source(s). Bsed on Pb isotope nlysis, Wong et l. (2002) reported tht soil Pb in the PRD region minly cme from vehicle exhust emissions. Whether the PC2 is derived from utomobile exhust emissions or nturl source(s) in griculturl res in the PRD region needs to be further investigted. The third principl component (PC3) represents 17.8 % of the totl vrince nd is dominted by Cd (0.621) nd negtively correlted with Pb ( 0.638). Due to cidic soil ph condition nd ctive phosphorus leching, phosphte fertilizers re commonly used in the red-soil res in the PRD region (Zhng nd Ke 2004; Wong et l. 2002). Becuse phosphte fertilizers contin lrge mount of Cd, the ppliction of phosphte fertilizers could result in substntil increses in the soil Cd concentrtion (Li et l. 2004). Therefore, we ssign the PC2 to fertilizer source. The effect of soil ph on hevy metl ccumultion in vegetbles In trget griculturl res of the PRD region, soil ph rnged from 4.51 to 7.85 nd verged 6.31 (medin, 6.45). Of the 92 soil smples, 63 hd ph vlues less

9 Environ Monit Assess (2014) 186: Tble 5 The prmeters used in the trget hzrd quotient clcultion of hevy metls vi vegetble consumption for the residents in the PRD region, South Chin Mening Unit Vlue Reference Adults Children EF Exposure frequency d/ USEPA (2002) ED Exposure durtion A Bennett et l. (1999), Chin (2012) IR Dily intke of vegetble for inhbitnt of PRD g/person/d M et l. (2005) fv The rtio of consumption of locl vegetbles to totl consumption Unitless 0.85 M et l. (2005), Gungdong Sttistics Bureu (2012) f Rtio of lef vegetble to locl vegetble Unitless 0.7 M et l. (2005), Gungdong Sttistics Bureu (2012) fb Rtio of fruit vegetble to locl vegetble Unitless 0.3 M et l. (2005), Gungdong Sttistics Bureu (2012) BW Averge weight of locl residents kg Wng et l. (2005) AT Averge exposure time d 21,900 3,295 USEPA (2002) C Averge concentrtion of metls in vegetbles mg/kg See Tble 1 This study Θ Wter content of fresh vegetbles % 85 Bes et l. (1984) RfD Reference dose mg/(kg d) RfD(Hg)= USEPA (2002) RfD(Cd)= RfD(Pb)= RfD(Cr)= RfD(As)= thn 7.0. Results of frequency nlysis of soil ph showed tht there were 24, 25, 37 nd 6 soil smples with soil ph rnges of <5.5, , nd >7.5, respectively. Integrting these results indictes tht the PRD griculturl soils ws slightly to severely cidic. Results of Person correltion nlysis showed tht there were significnt correltions between soil ph nd BCF vlues of Hg, Cd nd As but not Pb or Cr in flowering Chinese cbbge (Tble 4). Thus, soil ph condition my ply n importnt role in Hg, Cd nd As ccumultion while showing minor or no effect on Pb nd Cr uptke by flowering Chinese cbbge grown in griculturl res in the PRD region. The BCF vlues of Cd nd Cr in lettuce nd the BCF vlues of Pb in loose-lef lettuce were positively correlted to soil ph vlues (r=0.533, 0.574, nd 0.727, respectively; P< 0.05). In contrst, the BCF vlues of the five metls in pkchoi, Chinese cbbge nd Chinese lef mustrd hd no correltions with soil ph vlues. Our findings regrding the positive correltion between soil ph nd the BCF vlue of Cd in flowering Chinese cbbge s well s lettuce in griculturl re of the PRD region re inconsistent with the conclusions of Zho et l. (2009). Moreover, Dyton et l. (2006) reported tht ph hd no significnt effect on the ccumultion of Pb from soil into vegetbles, while Zeng et l. (2011) showed tht there ws significntly negtive correltion between soil ph vlues nd the EDTA-extrctble Cr, Cu, Fe, Mn, Pb nd Zn concentrtions. Overll, the effect of ph on the vilbility of hevy metls in soil nd their ccumultion behviors in vegetbles hs long been controversil (Wng et l. 2006, b; Eriksson 1989; McBride 2002), which needs further investigtions. In ddition to soil ph vlues, finer soil prticles (clys) hve greter ction exchnge cpcity (CEC) nd hence greter bility to retin ctionic metls thn sndy soils. Soil orgnic mtter (OM) plys n importnt role in ffecting metl biovilbility in soils s OM is mjor contributor to the phdependent negtive chrge in soils which gives rise to the soils bility to retin ctionic metls (McLughlin et l. 2011). Additionlly, dsorption nd complextion cn lso influence metl biovilbility in the soil. In the cse of exogenous contmintion, hevy metls re preferentilly dsorbed nd fixed in soil components with high specific surfce res, minly oxides, cly minerls, nd OM present in fine prticles (Chen et l. 2009; McLughlin et l. 2011).

10 1556 Environ Monit Assess (2014) 186: Tble 6 Trget hzrd quotient vlues (men ± stndrd devition) of hevy metls vi vegetble consumption for the residents in the Perl River Delt region, South Chin Hg Cd Pb Cr As Totl THQ Flowering Chinese cbbge Adult ± ± ± ± ± ±0.060 Child ± ± ± ± ± ±0.096 Lettuce Adult ± ± ± ± ± ±0.040 Child ± ± ± ± ± ±0.064 Pkchoi Adult ± ± ± ± ± ±0.117 Child ± ± ± ± ± ±0.188 Chinese cbbge Adult ± ± ± ± ± ±0.111 Child ± ± ± ± ± ±0.177 Loose-lef lettuce Adult ± ± ± ± ± ±0.086 Child ± ± ± ± ± ±0.138 Chinese lef mustrd Adult ± ± ± ± ± ±0.039 Child ± ± ± ± ± ±0.063 Men THQ of lef Adult ± ± ± ± ± ±0.077 vegetbles Child ± ± ± ± ± ±0.123 Potentil helth risk ssocited with consumption of lef vegetbles The potentil helth risks were ssessed using THQ, which were clculted ccording to Eqs 1 nd 2. The prmeters used in the equtions were listed in Tble 5.The potentil helth risk to locl residents ssocited with vegetble consumption ws ssessed with the THQ index (Tbles 6). Of the five hevy metls, As posed the gretest helth risk to dults nd children in the PRD study res, followed by Cr,Cd,PbndHg(Hg<Pb<Cd<Cr<As)(Fig.4). For both children nd dults, the THQs of hevy metls in the six lef vegetbles were less thn 1.0 (Tble 6), indicting tht the residents in the PRD region were not exposed to significnt helth risks ssocited with consumption of locl lef vegetbles. In ddition, the helth risks of hevy metl exposure to PRD residents vried in different lef vegetbles. Of the five metls, Hg nd Cr hd the lowest THQs in pkchoi, wheres the other metls (Cd, Pb nd As) hd the lowest THQ vlues in Chinese lef mustrd. In the six kinds of lef vegetbles, the THQs of Hg, Cd, Pb, Cr nd As were highest in Chinese lef mustrd, flowering Chinese cbbge, loose-lef lettuce, Chinese cbbge nd loose-lef lettuce, respectively (Tble 6). THQ dult child totl THQ b As Cr Pb Cd Hg Hg Cd Pb Cr As Metls 0.00 dult child Exposed popultions Fig. 4 The trget hzrd quotient (THQ)() nd totl THQ (b) of five hevy metls to children nd dults vi vegetble consumption in the Perl River Delt region, South Chin

11 Environ Monit Assess (2014) 186: The totl THQs of helth risk to children nd dults in the PRD region with consumption of lef vegetbles were nd 0.130, respectively (Fig. 4b). Thus, the residents in the PRD region were exposed to miniml risks ssocited with consumption of lef vegetble. Although the children s verge dily intke of vegetble only ccounts for 72.4 % of the dults intke, the totl THQ of hevy metls for children ws pproximtely 1.6-fold tht for dult. Thus, the children re more sensitive to hevy metl exposure through locl vegetble consumption thn dults in griculturl res in the PRD region. The THQ vlues of As, Cr, Cd, nd Pb ccounted for 50.1, 19.3, 16.0, nd 12.4 % of the totl THQs, respectively, while tht of Hg ccounted for smll portion only, ~2.17 %. These results indicte tht As, Cr, Cd nd Pb primrily impose helth risks to the resident in the study re, while Hg hs minor contribution to humn helth risks. The totl THQs of metls in lef vegetbles for children nd dults in the PRD region (0.208 nd 0.130) were fr below those of mrket vegetbles in Chongqing where even single metl s THQ hs exceeded the totl THQ (e.g., THQ of Pb for dults were ) (Yng et l. 2011) nd Beijing (0.771 nd 0.605) (Song et l. 2009). It should be noted tht the present study only estimted the helth risk of hevy metls to the residents vi consumption of locl lef vegetbles, which ccounts for 70 % of totl vegetble consumption in the PRD region. Tht is, this work only tkes into ccount prt but not the totl risks to PRD residents ssocited with consumption of vegetbles. In ddition, the totl risks of hevy metls re relted to the min polluted metls, nd their long-term interctions which cn impose distinct ecologicl or helth risks vi ntgonistic, dditive, nd/or synergistic effects (Menzie et l. 2009; Nordberg et l. 2005) were not considered. Thus, the potentil helth risks of hevy metl exposure to locl residents through consumption of lef vegetbles might be underestimted. Conclusions In the griculturl res of the PRD region, pkchoi hd the lowest cpcity for metl enrichment mong the six lef vegetbles under study. Of the five hevy metls, Cd ws more esily trnsferred from soil unto lef vegetbles, with BCFs ~30-fold those of Hg nd 50-fold those of Cr, Pb nd As. The min metl sources for lef vegetbles in the PRD griculturl res might include sewge irrigtion nd chemicl fertiliztion. Despite the significnt correltion between BCF nd soil ph vlues in specific smples, there is no cler reltionship between these two prmeters in ll smples s whole. The chrcteristics of hevy metl ccumultion in crops nd ssocited griculturl soil conditions need to be comprehensively considered for pproprite formultion of griculturl plnting plns. Despite certin degree of metl enrichment in soils nd vegetbles, the PRD residents were not experiencing significnt helth risk of hevy metl exposure through consumption of locl lef vegetbles in griculturl res. Still, more ttentions should be pid to children due to their higher sensitivity to hevy metl exposure thn tht of dults. Acknowledgments The reserch ws finncilly supported by the Ntionl Nturl Science Foundtion of Chin (no nd no ), the Gungzhou Municipl Technology Support Progrm (no. 2012J ), the Gungdong Provincil Reserch & Development Project (no. 2011B nd no. 2011B ), the Science nd Technology Plnning Project of Gungzhou (no. 2013J ), nd Nturl Science Foundtion of Gungdong province (no. S nd no. S ). Open Access This rticle is distributed under the terms of the Cretive Commons Attribution License which permits ny use, distribution, nd reproduction in ny medium, provided the originl uthor(s) nd the source re credited. References Adms, M. L., Zho, F. J., McGrth, S. P., Nicholsonb, F. A., & Chmbersb, B. J. (2004). Predicting cdmium concentrtions in whet nd brley grin using soil properties. Journl of Environmentl Qulity, 33, Álvrez-Ayuso, E., Otones, V., Murciego, A., Grcí-Sánchez, A., & Regin, I. S. (2012). Antimony, rsenic nd led distribution in soils nd plnts of n griculturl re impcted by former mining ctivities. Science of the Totl Environment, 439, Bdwy,S.H.,Hell,M.I.D.,Chudri,A.M.,Lwlor,K.,& McGrth, S. P. (2002). Soil solid-phse controls led ctivity in soil solution. Journl of Environmentl Qulity, 31, Bes, C. F., III, Shrp, R. D., Sjoreen, A. L., & Shor, R. W. (1984). A review nd nlysis of prmeters for ssessing trnsport of environmentlly relesed rdionuclides through griculture. Ok Ridge: Ok Ridge Ntionl Lbortory. Bennett, D., Kstenberg, W., & McKone, T. (1999). A multimedi, multiple pthwy risk ssessment of trzine: the impct of ge differentited exposure including joint uncertinty nd vribility. Relib Eng Syst Sfe, 63,

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