J Sci Food Agric 1997, 73, 446È454

Plant Availability of Heavy Metals in SoilsPreviously Amended with Heavy Applications ofSewage SludgeP S Hooda*

Department of Geography, Queen Mary and WestÐeld College, University of London, Mile End Road,London E1 4NS, UK

D McNulty

Biomathematics and Statistics, Scotland, Hannah Research Institute, Ayr KA6 5HL, UK

B J Alloway

Department of Soil Science, University of Reading, PO Box 233, Reading RG6 6DW, UK

and M N Aitken

Department of Environmental Science, SAC, Auchincruive, Ayr KA6 5HW, UK

(Received 25 July 1996 ; accepted 2 October 1996)

Abstract : Plant uptake is one of the major pathways by which sludge-bornepotentially toxic metals enter the food chain. This study examined the accumula-tion of Cd, Cu, Ni, Pb and Zn in wheat, carrots and spinach grown on soils from13 sites previously amended with sewage sludge. Winter wheat, carrots andspinach were grown consecutively under Ðeld like conditions. The results showedthat plant availability of heavy metals di†ered widely among the crop species.The accumulation of Cd, Ni and Zn in the plants showed the greatest increasescompared to their background levels. The Cu and Pb accumulation in the plantsgrown on sludge-amended soils showed only small increases compared to thosegrown on uncontaminated soils. Multiple regression analysis of various soilproperties showed that the surest way to control the accumulation of metals infood plants is by controlling their concentrations in the soils. Furthermore, soilswith a non-acidic pH and a clayey texture tended to achieve better control ofmetal accumulation in food plants compared to those with an acidic reactionand a coarse texture. Metal concentrations in the plants generally correlated wellwith those extracted from soils in 0É005 M DTPA, 0É05 M EDTA-(Na) 1 M2 ,

and 0É05 M The EDTA, however, proved to be a more reliableNH4NO3 CaCl2 .and consistent test in predicting the accumulation of metals in the plants. Theresults also showed that liming soils to pH 7 e†ectively reduced the metal con-tents in carrots and spinach, but liming to pH 6É5 had little e†ect on metalconcentrations in wheat grain.

Key words : plant availability, sludge-amended soils, metal contents, wheat,carrot, spinach, soil extractants, pH, soil type and liming.

* To whom correspondence should be addressed at : Institute of Environmental and Biological Sciences, Lancaster University,Lancaster, LA1 4YQ, UK.

446J Sci Food Agric 0022-5142/97/$09.00 1997 SCI. Printed in Great Britain(

Plant availability of heavy metals in soils 447

INTRODUCTION

Currently some 42% of the total sewage sludge produc-ed in the UK is diposed of by application to agricultu-ral land (DoE 1993). With increasing environmentalconcern, which has outlawed sea disposal by 1998 (CEC1991), sewage sludge utilisation in agriculture is likely toincrease in future years. Sewage sludge contains con-siderable amounts of N and P. In addition, it may alsocontain high concentrations of potentially toxic ele-ments (PTEs), particularly heavy metals (eg Cd, Cu, Ni,Pb, Zn). While sewage sludge recycling to agriculturalland is generally recognised as a fertiliser resource(Coker et al 1987), the contamination of soils withsludge-borne heavy metals continues to be an area ofconcern because of their persistence in the soils andtheir increased uptake by crop plants many years aftersludge applications have ceased (McGrath 1987).

Plant uptake is one of the major pathways by whichsludge-borne PTEs enter the food chain (Chaney 1990).Although a large body of research exists on factors con-trolling the uptake of these elements by crop plants (seethe review by Alloway and Jackson 1991), the conclu-sions drawn have tended to be based on studies con-ducted on soils recently treated with sludge. After theterminal sludge application, the soil will graduallyestablish a new biochemical equilibrium due to thedecomposition of sludge-added organic matter and, inmany cases, acidiÐcation of the soil. Consequently, theplant availability of sludge-borne elements may changeafter the biodegradation of sewage sludge in soils(Robertson et al 1982 ; Hooda and Alloway 1993).

Liming soils o†ers a means of minimising the risk offood chain contamination by reducing the plant uptakeof sludge-borne heavy metals (Williams et al 1987 ;Jackson and Alloway 1991 ; Smith 1994). Severalstudies, however, have indicated that liming may notalways have a signiÐcant e†ect, and that the e†ec-tiveness of liming could also vary depending on the soil,metal, pH value of the limed soils and crop species(Hemphill et al 1982 ; Pepper et al 1983 ; Kuo et al 1985 ;Eriksson 1989). Furthermore, the e†ect of liming onplant metal uptake from recently sludge-applied soilsmay also be confounded due to a possible progressiveacidiÐcation of the soil during the period of sludge bio-degradation.

Research on the behaviour of metals in soils whichhave stabilised after sludge applications is thereforeneeded to understand the long-term e†ects of sludgedisposal on agricultural land. This paper reports studiesconducted on 13 sludge-amended soils which hadequilibrated in the Ðeld for several years after sludgeapplications. The speciÐc objectives of the studies wereto :

(i) compare the uptake behaviour of Cd, Cu, Ni,Pb and Zn by wheat, carrots and spinach ;

(ii) examine the relation of various soil propertiesto metal contents in the plants ;

(iii) test the suitability of four soil extractants in pre-dicting metal uptake by crop plants ; and

(iv) study the e†ect of liming on plant metal con-tents.

MATERIALS AND METHODS

Samples of 13 soils, c 50 kg, previously amended withlarge quantities of sewage sludge over many years werecollected from various sites in the UK. In addition,similar samples of nine uncontaminated soils were alsoincluded for measuring the background levels of metalsin the food crops. All soil samples were passed througha coarse sieve (\5 mm) and divided into two equalhalves before being put into polyethylene tubs. The tubswere kept in the Ðeld in a rural location near Brent-wood in Essex (UK). Winter wheat (T riticum aestivumL), carrots (Daucus carota L) and spinach (Spinaciaoleracea L) were grown consecutively between 1989 and1991. All crops received a pre-sowing basal dressing ofan inorganic fertiliser supplying 60, 26 and 50 kg N, Pand K ha~1, respectively.

Of the 13 sludge-amended soils, nine (soil numbers1È9, Table 1) were acidic in reaction, and one replicateof these acidic soils was limed to pH 7 in 1987. Winterwheat was grown on soils which had been limed twoyears previously, and the pH of these soils averaged 6É5when measured after harvesting the wheat crop. Soilswhich showed a decrease in pH values were re-limed topH 7 again before sowing of carrots and spinach.

All crops were harvested at maturity. The edible partsof wheat (grain), carrot (roots) and spinach (leaves) werethoroughly washed with de-ionised water before beingdried in an oven at 65¡C. The samples of plant materialwere Ðnely ground in a centrifugal ball mill before beingdigested in concentrated AristaR grade follow-HNO3ing the procedure described in Jackson and Alloway(1991).

Soil particle size fractions were quantitatively deter-mined by the pipette method (Day 1965). Soil pH valueswere measured in water (Avery and Bascomb 1974). Thecontents of free iron oxides in soils were extracted withsodium dithionate (Avery and Bascomb 1974), andhydroxylamine hydrochloride was used for the extrac-tion of hydrous manganese oxides (Chao 1972). Soilorganic matter and cation exchange capacity weremeasured using the standard procedures described inHesse (1971).

The “plant availableÏ metal concentrations in soilswere extracted using 0É005 M DTPA (Lindsay andNorvell 1978), 0É05 M EDTA-(Na) (Anon 1986), 1 M2

and 0É05 M (Alloway and MorganNH4NO3 CaCl2

448 P S Hooda et al

TABLE 1Heavy metal contents and selected physico-chemical characteristics of soilsa

Soil number Metal concentration (mg kg~1) Clay OM pH CEC FFeO HMnO CaCO3 L ast sludge(%) (%) (cmol

ckg~1) (%) (mg kg~1) (%) application

Cd Cu Ni Pb Zn

1 4É35 86É4 65É2 85É9 221É0 31É0 5É6 6É65 17É9 1É55 444É8 1É5 19852 10É40 199É8 121É4 177É5 497É5 29É8 5É6 6É15 18É7 1É24 315É2 1É9 19853 0É71 148É0 49É5 902É5 322É5 46É1 4É3 5É11 29É6 1É15 195É6 2É7 19844 12É30 164É9 45É2 200É9 485É3 44É2 17É5 5É54 41É9 0É57 75É9 41É5 19845 5É07 72É5 13É1 149É7 150É0 18É0 3É3 6É35 19É4 1É04 128É8 2É8 19826 7É30 119É2 44É3 107É6 291É6 33É3 5É9 5É50 35É1 2É16 95É6 2É5 19797 8É07 884É0 103É7 813É7 1125 26É6 13É8 6É09 42É3 1É12 139É9 5É9 19878 3É35 41É1 51É6 63É5 346É0 28É0 4É5 5É81 20É0 1É30 91É7 1É9 19789 1É57 187É4 53É2 200É8 462É5 81É0 11É0 6É40 45É8 3É11 70É4 3É2 1988

10 2É45 210É5 42É0 450É5 370É0 45É3 22É5 6É96 48É2 2É66 292É0 4É9 198411 2É40 68É4 32É8 42É0 170É0 41É5 5É0 7É29 35É5 2É08 95É6 2É9 198512 7É40 102É2 40É8 92É6 260É0 20É5 4É1 7É04 18É3 4É70 598É7 3É0 197913 3É82 85É0 11É2 85É0 202É5 19É5 4É6 7É30 22É4 0É46 292É9 64É0 197614 0É49 30É8 21É8 75É2 82É3 40É9 38É2 6É60 126É2 1É27 86É2 65É2 NCSS15 0É73 29É9 21É9 79É5 128É7 30É5 5É7 6É04 21É8 1É20 581É9 2É0 NCSS16 0É49 15É6 18É5 22É3 37É3 28É5 4É5 7É37 22É6 2É09 357É8 26É0 NCSS17 0É49 19É4 28É1 44É1 75É8 60É5 11É5 7É21 41É8 0É80 370É1 24É9 NCSS18 0É52 126É5 39É2 268É5 158É0 20É0 18É1 4É42 47É3 2É45 108É8 1É2 NCSS19 0É40 24É2 30É2 32É5 126É2 48É7 4É7 6É90 35É2 2É21 73É7 2É4 NCSS20 0É30 14É5 4É8 36É0 95É2 20É3 4É1 7É42 21É5 0É46 329É8 8É2 NCSS21 0É46 16É7 8É5 45É0 182É3 28É6 3É8 4É70 23É4 1É27 83É2 1É5 NCSS22 0É46 16É5 29É2 23É5 124É6 32É8 4É0 4É20 21É8 3É07 266É7 1É0 NCSS

a Abbreviations : OM, organic matter ; CEC, cation exchange capacity ; HMnO, hydrous manganese oxides ; FFeO, free Fe oxides ;NCSS, no history of contamination with sewage sludge.

1985). For total metal concentrations, soil samples weredigested in a mixture of and HF. The metal con-HClO4centrations in food and soil samples were determinedusing Ñame atomic absorption spectrometry or electro-thermal atomisation atomic absorption spectrometryfor very low metal concentrations.

RESULTS AND DISCUSSION

The concentrations of metals in many of the soils usedin this study are higher than the maximum permissiblevalues under the current European Union regulations(CEC 1986). For this reason the data from this studymay not be suitable for considerations of dietary metalintake scenarios. However, sludge-amended soils whichhave equilibrated in the Ðeld for many years provide avaluable means of studying the soil-plant relationshipsof PTEs. The soils used in these experiments di†eredwidely in physico-chemical properties, metal composi-tion and history of sludge application (Table 1). Theresults from this study were therefore expected to be ofwider applicability and more useful than those stem-ming from similar studies conducted on a few freshlysludge-amended soils.

Metal concentrations in wheat, carrots and spinach

The concentration of metals in the dry matter of wheatgrain, carrot roots and spinach leaves produced on thesewage sludge-amended and uncontaminated soils aresummarised in Table 2. While the concentrations of Cdand Ni in wheat grain grown on the sludge-amendedsoils were much greater than their concentrations inthose produced on the uncontaminated soils, Pb andZn concentrations in wheat grown on the sludge-amended soils were only marginally higher (Table 2).The observed mean concentrations of 0É32 mg kg~1 forPb and 47É6 mg kg~1 for Zn in wheat grain fromsludge-amended soils, however are common for wheatcrops grown on soils not contaminated with sewagesludges (Vigerust and Selmer-Olsen 1986 ; Lu� bben andSauerbeck 1991). The mean Cu concentration(3É90 mg kg~1) in wheat grain produced on the sludge-amended soils appeared to be rather lower than itsbackground level (4É17 mg kg~1).

The mean concentrations of Cd, Ni and Zn in carrotsfrom the sludge-amended soils were very much higherthan those grown on the uncontaminated soils (Table2). The concentrations of Cu and Pb in carrots produc-ed on the sludge-amended soils were also elevated com-pared to their background levels, but the increases were

Plant availability of heavy metals in soils 449

TABLE 2Contents of Cd, Cu, Ni, Pb and Zn (mg kg~1 DW) in wheat,carrots and spinach produced on uncontaminated and sludge-

amended soils, and their soil-to-plant transfer coefficients

Element Uncontaminated Sludge contaminatedsoils (n \ 9) soils (n \ 13)

Mean T ransfer Mean T ransferratioa ratioa

W heat grainCadmium 0É24 0É451 0É68 0É112Copper 4É17 0É189 3É90 0É031Nickel 0É58 0É051 2É15 0É034Lead 0É23 0É006 0É32 0É002Zinc 47É62 0É412 58É35 0É133

Carrot rootsCadmium 0É63 1É204 1É71 0É350Copper 5É18 0É249 7É23 0É058Nickel 2É17 0É185 5É28 0É118Lead 0É33 0É009 0É48 0É004Zinc 25É48 0É278 41É74 0É132

Spinach leavesCadmium 0É94 2É092 12É76 1É991Copper 9É48 1É806 16É91 0É156Nickel 4É76 0É462 9É46 0É178Lead 0É82 0É020 0É95 0É008Zinc 206É0 2É297 455É5 1É216

a Transfer ratio \ plant metal concentration/soil metal con-centration.

relatively small compared to those observed for Cd, Niand Zn (Table 2). The observed average concentrationsof 7É23 mg kg~1 for Cu and 0É48 mg kg~1 for Pb incarrots grown on the sludge-amended soils, however arewithin the ranges reported for carrots grown on soilsnot contaminated with sewage sludges (Keefer et al1986).

Spinach leaves grown on the sludge-amended soilsaccumulated substantially higher metal contents thanthose grown on the uncontaminated soils. Spinachgrown on the sludge-amended soils, on an average,absorbed more than 13-times as much Cd, more thantwice as much Zn and Ni and nearly twice as much Cucompared to their background levels in plants on theuncontaminated soils (Table 2). The concentration ofPb in spinach leaves produced on sludge-amended soilsshowed only a small increase compared to its back-ground level (Table 2).

Spinach tissues accumulated the highest concentra-tions of all Ðve metals, while wheat grain accumulatedthe lowest concentrations of Cd, Cu, Ni and Pb amongthe three crops ; the lowest Zn concentration was incarrot roots (Table 2). The sequence of metal concentra-tions in the plant tissues from sludge-amended soils wasZn[ Cu[ Ni[ Cd[ Pb for wheat grain and carrot

roots, and Zn [ Cu[ Cd [ Ni[ Pb for spinachleaves. The concentrations of metals in wheat, carrotsand spinach grown on sludge-amended soils in thisstudy clearly showed that metal uptake is plant-speciesdependent. The Ðndings are consistent with thosereported in the literature (Schauer et al 1980 ; Keefer etal 1986 ; Vigerust and Selmer-Olsen 1986 ; Lu� bben andSauerbeck 1991 ; Sauerbeck 1991 ; Smith 1994).

The metal uptake data also showed that soil-to-planttransfer of metals varied widely among wheat, carrotsand spinach. Soil-to-plant metal transfer ratios (ratio ofthe concentration of a metal in plants to its concentra-tion in the soil) were much higher for spinach than forwheat and carrots, and this was consistent with all Ðvemetals (Table 2). This implies that, for a given level ofmetals in soils, spinach leaves accumulate far greateramounts of metals than wheat grain and carrot roots.Overall, the amounts of Cd, Ni and Zn in the foodplants showed the greatest increases compared to theirbackground levels. The concentrations of Cu and Pb inthe plants grown on the sludge-amended soils were alsoelevated, but to a much less extent. This is primarilybecause of their very low soil-to-plant transfer ratioscompared to those of Cd, Ni and Zn (Table 2). Plantuptake is one of the major pathways by which metalsfrom sludge-amended soils enter the food chain. Thefood-chain plants might absorb enough amounts ofheavy metals to become a potential health hazard toconsumers. In this context, the results showed that Cd,Ni and Zn pose the greatest threat among the metalsstudied because the levels of Cu and Pb were eitherrelatively low or did not show any appreciable increasecompared to their background concentrations in thefood crops.

Soil factors a†ecting metal accumulation in plants

The inÑuence of various soil properties on metal con-centrations in wheat, carrots and spinach was evaluatedinitially by stepwise multiple regression analyses andinvolved all the soil variables mentioned in Table 1. Soiltotal metal concentration was found to be the principalfactor controlling metal contents in the plants, and wasthe only factor which consistently appeared in allmodels. The inclusion of other soil variables, such aspH, cation exchange capacity (CEC), organic matter,iron and manganese oxides and texture (clay), in themodels gave results which were inconsistent and some-what ambiguous. It is well known that many soildescriptors (eg CEC and texture or CEC and organicmatter) are highly correlated and this may be one of thereasons why the multiple stepwise regression gaveinconsistent results. To overcome the problems associ-ated with correlated descriptors the soil variables weremapped onto an uncorrelated set of predictors formedby principal component analysis (PCA) of the soil vari-ables. The stepwise regression was repeated using the

450 P S Hooda et al

new uncorrelated variables and the regression equationback transformed to the original variables. The backtransformed regression equations were then used toidentify a small set of independent soil descriptors forinclusion into Ðnal equations. All calculations were per-formed using Genstat 5 (release 3.1 copyright ; LawesAgricultural Trust, Rothamsted Experimental Station,UK). The PCA results indicated that total metal, pHand clay content were inÑuential in most stepwiseregression equations. Consequently it was decided thatthe Ðnal regression equation ought to consist of threesoil descriptors ie total metal concentration, pH andclay fraction. The multiple regression equations describ-ing the relationships between metal concentrations inplants and these three soil variables are given in Table3. The results show that the relationship between metaluptake in plants and the soil variables in the regressionmodel is strongly inÑuenced by metal and plant species.For example, this model accounts for 62, 91 and 67%,respectively, of the variation in Cd uptake data forcarrots, spinach and wheat (Table 3).

Regression coefficients with relatively small standarderrors of estimate (SE), ie with a high t-ratio (coefficient/SE) indicate that a particular variable has a strong e†ecton the uptake of a metal in a plant. The coefficients fortotal metal concentration generally had the lowest SEvalues (data not given) among the three soil variables inthe model. This means that the concentration of a metalin soils is the principal factor for predicting its concen-tration in carrots, spinach and wheat. The relativelysmall regression coefficients (Table 3) with somewhat

large SE values for clay fraction, as compared with pH,suggest that the soil clay fraction does not predict metalaccumulation in plants as well as pH. Obviously the pHis more important than clay content in regulating theplant availability of these metals in the soils used in thisstudy. The e†ect of organic matter, CEC, free Fe oxidesand hydrous Mn oxides on metal accumulation in theplants was less clear. This may be partly due to thelarge variability in metal concentrations in these soils(Table 1). Had the concentrations of the metals beensimilar across all soils, these soil variables would poss-ibly have also a†ected metal accumulation in the plantsin a more clear manner. These results however are con-sistent with a study conducted under similar conditionsinvolving soils from 13 long-term Ðeld experiments(Sauerbeck 1991). The author found that organic matterand texture are less important than the metal concen-trations in soils and pH in regulating the availability ofCd, Cu, Ni and Zn to several crop plant species.

From the above discussion it could be concluded thatalthough metal accumulation in plants is stronglya†ected by their concentrations in soils, metal avail-ability to plants varies with soil type. Plants grown onsoils with pH values in the neutral range and a clayeytexture tend to accumulate less metals than those grownon soils with an acidic pH and a coarse texture. Thismeans disposal of sewage sludge on clayey texturedsoils with either a neutral to alkaline pH or combinedwith lime treatment might help achieve better control ofmetal accumulation in food plants grown on sludge-amended soils.

TABLE 3Multiple regression equationsa for plant metal content (mg kg~1) in relation to total soil metal

concentration (mg kg~1), pH and soil clay fraction (%)

Equation R2 P-value

CarrotsCd \ 3É44 ]0É284 soilÈCd [0É328 pH [0É017 clay 0É622 0É008Cu \ 11É06 ]0É018 soilÈCu [1É179 pH ]0É018 clay 0É836 \0É001Ni \ 5É20 ]0É218 soilÈNi [0É450 pH [0É097 clay 0É838 \0É001Pb \ 1É164 ]0É009 soilÈPb [0É123 pH ]0É0004 clay 0É582 0É012Zn \ 43É50 ]0É068 soilÈZn [3É80 pH ]0É027 clay 0É725 0É002

SpinachCd \ 29É43 ]1É919 soilÈCd [3É93 pH [0É087 clay 0É910 \0É001Cu \ 50É20 ]0É014 soilÈCu [4É83 pH [0É133 clay 0É626 0É007Ni \ 6É80 ]0É185 soilÈNi [1É00 pH ]0É028 clay 0É723 0É002Pb \ 0É601 ]0É0016 soilÈPb ]0É011 pH ]0É0023 clay 0É911 \0É001Zn \ 829 ]0É342 soilÈZn [64É10 pH [4É82 clay 0É383 0É045

W heatCd \ 0É990 ]0É183 soilÈCd [0É156 pH [0É003 clay 0É672 0É012Cu \ 6É65 ]0É002 soil [ Cu [0É503 pH [0É021 clay 0É664 0É013Ni \ 0É344 ]0É082 soilÈNi [0É051 pH [0É029 clay 0É761 0É004Pb \ 0É712 ]0É0008 soilÈPb [0É047 pH [0É0059 clay 0É759 0É004Zn \ 208 ]0É019 soilÈZn [24É86 pH [0É024 clay 0É595 0É025

a Based on data from 13 sludge-amended soils.

Plant availability of heavy metals in soils 451

Soil extractants and metal concentrations in plants

The concentrations of Cd, Cu, Ni, Pb and Zn in theedible parts of carrots, wheat and spinach were reg-ressed against the concentrations of trace elementsextracted with the four chemical reagents (0É005 M

DTPA, 0É05 M EDTA-(Na) 1 M and 0É05 M2 , NH4NO3Cadmium extracted with all the four extractantsCaCl2).

correlated signiÐcantly with Cd contents in each of thecrops. However, Cd concentrations in spinach were bestpredicted by the DTPA and those in carrots and wheatby the EDTA (Table 4). Similarly, Cu contents in theplant tissues were signiÐcantly related to soil Cu con-centrations extracted by all the four reagents but DTPAfor carrots, for spinach and for wheatNH4NO3 CaCl2gave the best relationships among the four extractantsemployed (Table 4). For Ni concentrations in planttissues, all the four soil extractants gave highly signiÐ-cant relationships but the concentrations were best pre-dicted by the for carrots, EDTA for spinach andCaCl2

for wheat (Table 4).NH4NO3The Pb concentrations in the plants were best pre-

dicted by the EDTA test (Table 4). Soil Pb concentra-tions extracted in and were not foundCaCl2 NH4NO3to be related to Pb contents in the crop plants. This ispartly due to the fact that the Pb concentrationsextracted by these neutral salt solutions were frequently

near the detection limit (0É05 mg dm~3) of the Ñameatomic absorption spectrometer (FAAS) used. It wouldappear, therefore, that the and extract-NH4NO3 CaCl2ants may well be suitable for predicting Pb availabilityto plants if a more sensitive analytical method becameavailable. The Zn concentrations in both spinach andwheat were best predicted by those extracted from thesoils with the solution, only in carrots was the ZnCaCl2concentration better related to the EDTA-extractableZn (Table 4).

In general, the ability of the extractants to predictplant-available metals depended on the crop species, themetal and extractant used. Overall, the results showthat 0É05 M EDTA is a reliable test for predicting metalavailability to carrots, spinach and wheat from sludge-amended soils. This was because it was the only extract-ant which consistently correlated with all Ðve elementsin each of the crops and proved to be the best extract-ant in many cases (Table 4). EDTA and DTPA are themost commonly used soil tests for assessing plant-available metals, and, because of their greater extractingstrength, are likely to be more sensitive to reducedmetal solubilities at higher soil pH or to soils low inmetal contents. For a speciÐc metal or crop, however0É05 M or 1 M may provide a betterCaCl2 NH4NO3prediction than EDTA or DTPA. For example, the Niconcentrations in carrots and wheat were better predict-

TABLE 4Linear regression equations of the form y \ a ] bx where y represents metal concentration inthe edible plant tissues (mg kg~1) and x is the soil metal concentration (mg kg~1) extracted by

one of the four extractants used

y a SE b SE x R2 P

CadmiumCarrot 0É653 0É297 0É469 0É071 EDTA 0É781 \0É001Spinach 2É41 1É91 3É92 0É672 DTPA 0É734 \0É001Wheat 0É069 0É125 0É224 0É029 EDTA 0É855 \0É001

CopperCarrot 5É23 0É790 0É052 0É008 DTPA 0É769 \0É001Spinach 12É67 1É81 1É93 0É543 NH4NO3 0É493 0É004Wheat 2É40 0É187 1É21 0É218 CaCl2 0É752 \0É001

NickelCarrot 1É50 0É770 3É48 0É307 CaCl2 0É914 \0É001Spinach 4É52 1É37 0É301 0É047 EDTA 0É763 \0É001Wheat 0É453 0É137 1É52 0É080 NH4NO3 0É973 \0É001

L eadCarrot 0É327 0É097 0É002 0É0008 EDTA 0É433 0É009Spinach 0É698 0É089 0É004 0É0007 EDTA 0É711 \0É001Wheat 0É179 0É061 0É002 0É0005 EDTA 0É653 0É002

ZincCarrot 26É62 5É04 0É130 0É026 EDTA 0É663 \0É001Spinach 299É10 56É50 16É86 5É59 CaCl2 0É403 0É012Wheat 37É78 5É42 2É60 0É494 CaCl2 0É728 \0É001

a Based on data from 13 sludge-amended soils.

452 P S Hooda et al

ed by 0É05 M and 1 M respectively,CaCl2 NH4NO3 ,compared to the EDTA and DTPA (Table 4). Similarly,soil Ni concentrations extracted by neutral salts such as

(0É05 M), (1 M) and (1 M) wereCaCl2 MgCl2 NaNO3found to be better correlated with Ni contents in 13crop species compared to other extractants (EDTA,DTPA, (Sauerbeck and Hein 1991).NH4OAc, CuCl2)Indeed, metals extracted with a weaker extractant suchas 0É05 M or water would represent the most realCaCl2plant-available metals in soils. These extractants,however, have the disadvantage of extracting metals invery small concentrations which are often too low forFAAS, and are difficult to determine by ETAASbecause of the chloride matrix interference and possiblecontamination problems (Ure 1990). As a result, strong-er extractants such as DTPA and EDTA have beenmost widely used (Alloway and Jackson 1991). In thisstudy, 0É05 M EDTA-(Na) was found to be a better and2

consistent predictor of plant-available metals amongthose tested.

E†ect of liming on metal contents in the plant tissues

Figure 1(A) shows the e†ect of liming on soil pH values.The application of lime to soils signiÐcantly increasedsoil pH values. The e†ects of liming on metal concentra-tions in wheat, carrots and spinach are summarised inFigs 1(B)È(F). Liming the soils to pH 7 signiÐcantlyreduced the concentrations of all Ðve metals in carrotroots (Figs 1(B)È(F)). The metal concentrations incarrots grown on the limed soils were lower, on average,by 39% for Cd and Ni, 44% for Zn, 48% for Pb and28% for Cu compared to their concentrations in plantsgrown on the unlimed soils. Liming the soils to pH 7also decreased metal contents in spinach leaves. As with

Fig 1. E†ects of liming on soil pH values and accumulation of metals in wheat grain, carrot roots and spinach leaves. The errorbars represent the least signiÐcant di†erence (LSD, PO 0É05) between the two sets of data.

Plant availability of heavy metals in soils 453

carrots, the metal concentrations in spinach leaves pro-duced on the limed soils were reduced by 39% for Cd,27% for Cu, and more than 40% for Ni and Zn (Figs1(B)È(F)). The Pb concentration in spinach leaves,however showed a relatively small reduction of 19%due to liming (Fig 1(E)).

Winter wheat was grown on soils which had beenlimed two years previously, and the pH of these soilsaveraged 6É5 when measured after harvesting the wheatcrop. This pH was still statistically higher than that ofunlimed soils (Fig 1(A)), but had no consequential e†ecton the contents of Cd, Cu, Ni and Zn in wheat grain(Figs 1(B)È(F)). In contrast, however the wheat grainproduced on the limed soils had signiÐcantly lower con-tents of Pb than those on the unlimed soils (Fig 1(E)).

Liming sludge-amended soils to pHP 6É5 is oftenrecommended to minimise plant uptake of PTEs. Thereduction in metal concentrations in carrots andspinach due to liming the soils is consistent with theÐndings reported in the current literature (Eriksson1989 ; Jackson and Alloway 1991 ; Lu� bben and Sauer-beck 1991 ; Smith 1994), but the liming had no e†ect onmetal contents in wheat grain, except for Pb. The resultsindicate that while liming soils to pH 7É0 was e†ectivein reducing metal accumulation in carrots and spinach,liming to pH 6É5 had little e†ect on metal accumulationin wheat grain. This infers that either pH 6É5 was nothigh enough to have a substantial e†ect on metaluptake or that metal accumulation in wheat grain wasindependent of soil pH. Wheat straw samples were notanalysed for their metal contents in the present study.As a result, it is difficult to say whether liming to pH 6É5was not sufficient enough to have a signiÐcant reductionin wheat metal contents or metal translocation fromwheat vegetative parts to grain was independent of soilpH. Results from a recent study, however suggested thatmetal contents in reproductive plant parts, such asgrain, were independent of soil pH. For example, whileliming sludge-amended soils over a pH range of 3É9È7É6substantially reduced Cd concentrations in potatoes,ryegrass and oat straw, it had no e†ect on Cd contentsin oat grain (Smith 1994). The results from the presentinvestigation together with other recent studies (Smith1994) indicate that liming is less likely to control metalaccumulation in the seeds of cereal crops such as wheatand oat grain.

The Council of the European Communities has Ðxedmandatory concentrations for PTEs in soils receivingsewage sludge (CEC 1986). The maximum permissiblemetal concentrations in the 1986 EC Directive onsludge regulation (CEC 1986) apply to soils with pH inthe range of 6É0È7É0. Where sewage sludge is applied tosoils with pH values \6É0, Member States are requiredto reduce the maximum permissible concentrationsaccordingly to counterbalance the increased availabilityof metals to crop plants. In the UK, lower metal limitsapply for Cu, Ni and Zn where sludge is applied to soils

with pH values \6É0 compared to pH band 6É0È7É0(Statutory Instrument 1989). However, the maximumconcentration of Cd (3 mg kg~1) and Pb (300 mg kg~1)in the EC Directive of 1986 are permitted in sludge-amended soils with a pH value as low as 5É0 (StatutoryInstrument 1989), without taking account of theirpotentially increased bioavailability at lower pH values(\6É0). The results in this study clearly demonstrate anincreased uptake of heavy metals at lower soil pHvalues. This is particularly signiÐcant with regard to Cdand Pb which potentially can accumulate in humansfollowing ingestion of contaminated foods. The currentUK Regulations for both these metals take no accountof the soil pH and are at the highest level of themaximum range permitted in the European Unionregulations (CEC 1986). It would, therefore, be prudentto base maximum Cd and Pb loading values on the soilpH (as is the case with Cu, Zn and Ni).

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