Natural Attenuation of Zn, Cu, Pb and Cd in Three Biosolids-Amended Soils of Contrasting pH Measured...

Natural Attenuation of Zn, Cu, Pb and Cd in ThreeBiosolids-Amended Soils of Contrasting pH MeasuredUsing Rhizon Pore Water Samplers

Ghulam Murtaza & Richard John Haynes &

Ravindra Naidu & Oxana N. Belyaeva &

Kwon-Rae Kim & Dane T. Lamb & Nanthi S. Bolan

Received: 5 October 2010 /Accepted: 21 March 2011 /Published online: 5 April 2011# Springer Science+Business Media B.V. 2011

Abstract The effects of application of biosolids, atfour rates, to an alkaline (pH 8.4), neutral (pH 7.0)and acidic (pH 4.0) soil on concentrations of Cu,Zn, Pb, Cd and dissolved organic C in soil solutionwere measured over a 170-day period in a labora-tory incubation study using Rhizon pore watersamplers. Applications of biosolids decreased solu-tion pH in the alkaline soil, increased it in theacidic soil and had little effect in the neutral soil. Ingeneral, increasing application rates of biosolidsprogressively increased EC and concentrations ofdissolved organic C (DOC), Cu, Zn, and to a lesser

extent Cd and Pb, in soil solution. Concentrationsof DOC and concentrations of solution Cu, Zn, andto a lesser extent solution Cd and Pb, decreasedover the incubation period. In all three soils,concentrations of solution Cu and Zn were closelypositively correlated with DOC concentrations andsimilar positive but weaker correlations were foundfor solution Cd and Pb. For the alkaline and neutralsoils, concentrations of solution Cu, Zn, Cd and Pbwere generally negatively correlated with solutionpH but for the acidic soil, positive correlations forCu and Zn were recorded. The percentage reductionin solution Cu and Zn, between 0 and 170 daysincubation, increased with increasing rates of bio-solids in the acid soil (where biosolids applicationsincreased pH) but the reverse was the case for thealkaline soil (where pH fell following biosolidsapplications). Greatest percentage reduction insoluble Cu and Zn occurred in the neutral soilwhich had the greatest BET surface area, clay andorganic matter contents and therefore the greatestcapacity to adsorb heavy metal cations. It wasconcluded that solution pH, dissolved organic Cand the intrinsic capacity of the soil to removemetals from solution, were the main factors inter-acting to regulate heavy metal cation solubility inthe biosolids-amended soils.

Keywords Biosolids . Zn . Cu . Pb . Cd . Soil pH .

Dissolved organic C

Water Air Soil Pollut (2011) 221:351–363DOI 10.1007/s11270-011-0795-8

G. Murtaza :R. Naidu :K.-R. Kim :D. T. Lamb :N. S. BolanCentre for Environmental Risk Assessment andRemediation, Division of Information Technology,Engineering and the Environment,University of South Australia,Mawson Lakes Campus,Adelaide, South Australia 5095, Australia

G. Murtazae-mail: [email protected]

G. MurtazaInstitute of Soil and Environmental Sciences,University of Agriculture,Faisalabad 38040, Pakistan

R. J. Haynes (*) :O. N. BelyaevaSchool of Land, Crop and Food Sciences/CRC CARE,The University of Queensland,St. Lucia, QLD 4072, Australiae-mail: [email protected]

1 Introduction

Biosolids applications to soils result in a substantialsupply of macro (e.g. N, P, K) and micronutrients thatare essential to plants (Haynes et al. 2009). Inaddition, organic matter additions in biosolids canimprove soil aggregation, increase water retentioncapacity and promote soil microbial activity (Khaleelet al. 1981; Fernandes et al. 2005). However,biosolids can also introduce pathogens and organicand inorganic contaminants. Heavy metal contami-nants (e.g. Zn, Cu, Pb and Cd) are of particularconcern because they persist in the soil system almostindefinitely and, when oversupplied, they can be toxicto plants, soil biota and humans.

Natural attenuation is an important phenomenon inmetal-contaminated soils since it involves naturalprocesses (e.g. specific adsorption, precipitation andcomplexation) that act to reduce metal bioavailability(Yong and Mulligan 2003). Indeed, when inorganicsalts of heavy metals are added to soils, the highestvalue of solubility and plant availability is in theperiod immediately after application and with timebioavailabilty diminishes (i.e. an ageing effect) due tonatural attenuation (Hooda and Alloway 1993; Ma etal. 2006). The capacity for both the inorganic andorganic components of biosolids to adsorb metalsmeans that they are initially less soluble and bioavail-able than when the same rate of metals is applied inthe form of inorganic salts (Hooda and Alloway1993). Subsequent reactions in the soil are complex.For example, decomposition of biosolids organicmatter could release previously organically boundmetals into solution while soluble organic matter fromthe biosolids could increase metal solubility throughformation of soluble metal–organic matter complexes(Basta et al. 2005; Bolan et al. 2011). On the otherhand, easily soluble metals in biosolids might berapidly adsorbed by inorganic/organic soil compo-nents (Haynes et al. 2009). The effect of theinteraction of such effects is unclear and, indeed,surprisingly little research has examined the solubilityof metals in soils in the immediate period (e.g. first6 months) after biosolids application. Certainly, soilpH should have an important effect since biosolids-borne metals are characteristically less soluble andbioavailable in soils of high pH and/or after limeapplications (Alloway and Jackson 1991; Lombi et al.2003).

A wide variety of soil test extractants have beenemployed to determine heavy metal bioavailability(McLaughlin et al. 2000) including neutral salts, acidsand chelating agents. However, the most immediatemeasurement of metal bioavailability is the concen-tration of metals in soil solution. Several techniquesexist to sample pore water including displacement,centrifugation and use of suction cup samplers(ceramic or Teflon; Fares et al. 2009). In recent times,Rhizon pore water samplers (Meijboom and vanNoordwijk 1991) have been used successfully(Knight et al. 1998; Tye et al. 2003; Tiensing et al.2001: Sigfusson et al. 2006) and they are consideredmore inert than ceramic, and less expensive thanteflon samplers. The purpose of this study was useRhizon solution samplers to measure the extent ofnatural attenuation of biosolids-borne Zn, Cu, Pb andCd, over a 6-month period, following addition ofbiosolids to an acid, neutral and alkaline soil.

2 Materials and Methods

2.1 Soils and Biosolids Used

Three soils varying in physiochemical properties weresampled from Wallaroo, South Australia (alkalineCalcarosol; Isbell 2002), Mawson Lakes, SouthAustralia (neutral Dermosol), and Bribie Island,Queensland (acidic Podosol) from the 0–0.2 m layer.Biosolids were collected from the Bolivar WastewaterTreatment Plant (SAWater, South Australia). Soil andbiosolids samples were air-dried and sieved (<2 mm)prior to use.

2.2 Experimental Design

Soil samples (2 kg) were amended with increasingamounts of biosolids to achieve final biosolidsapplication rates of 0, 10, 20 and 30 gkg−1 soil andthe mixtures were then homogenised mechanically.These rates were based on a typical biosolidsapplication rate of 20 gkg−1 (which approximates to20 Mg ha−1 to a depth of 10 cm) and varied from 0.5to 1.5 times that rate. Samples were placed in plasticcontainers and pore water samplers with a pore size<0.2 μm (Rhizon Research Products, the Netherlands)were buried in each soil mixture. These consist of ahydrophilic porous polymer tube (typical pore diam-

352 Water Air Soil Pollut (2011) 221:351–363

eter=0.1 um) attached to a polyvinyl chloride tube(Meijboom and van Noordwijk 1991). Soils wererewetted to 70% water holding capacity and incubatedfor 170 days at room temperature. Containers wereopened periodically, weighed and water added whennecessary to maintain the predetermined soil watercontent. The experiment was replicated three times.

Pore water was extracted at time 0 and then at 4,10, 30, 50, 75, 110, 140 and 170 days. Sufficient porewater was collected to determine pH, electricalconductivity (EC), dissolved organic carbon, Zn, Cu,Cd and Pb.

2.3 Soil Analysis

Soil pH and EC were measured in a 1:5 soil/watersuspension. Soil organic carbon was determined bythe Walkley–Black method (Rayment and Higginson1992). Ash content of the biosolids was determinedby igniting at 700°C for 4 h. Soluble C was measuredin aqueous extracts (1:5 soil/water ratio for 16 h) afterfiltration through a 0.45 μm Millipore filter using atotal carbon analyzer (1010 OI Analytical). Totalconcentrations of Cu, Zn, Cd and Pb were determinedin duplicate following microwave digestion usingaqua regia (1 HNO3/3 HCl) (USEPA 2005). It isaccepted that this method does not necessarily digest100% of the aluminosilicate soil matrix and thereforemay underestimate total metal content by up to 5%(Sastre et al. 2002). Samples were filtered through0.45 μm Millipore filters before analysis by induc-tively coupled plasma-mass spectroscopy (ICP-MS).The clay, sand and silt contents were determinedfollowing the micro pipette method (Miller and Miller1987). Specific surface area was measured by theBET method (Brunauer et al. 1938) on a Gemini 2380surface analyser. Effective cation exchange capacitywas determined by summation of 1 M ammoniumchloride-extractable K, Ca, Mg and Al by ICP-MS(Rayment and Higginson 1992). Free Fe and Al oxideswere measured by ICP-MS after extraction withdithionite-citrate solution (Rayment and Higginson1992).

Immediately following mixing of the treatments,samples were taken (along with biosolids alone) andpH buffer curves were constructed. Increasing vol-umes of 0.2 M NaOH or HCl were added to 10 g soilalong with enough distilled water to give a finalsample/solution ratio of 1:2.5. Samples were stirred

for 40 min and the pH was then measured. Prelimi-nary heavy metal analysis of centrifuged suspensionsfrom the buffer curve for the biosolids showeddifferent trends for different metals. As a result, theexperiment was repeated in a background solution of0.01 NaNO3 (in order to maintain constant ionicstrength) using NaOH and HNO3 to adjust pH.Concentrations of dissolved organic C, Cu, Zn, Cdand Pb in centrifuged solutions were analysed asdescribed below for pore water extracts.

2.4 Pore Water Analysis

Pore water pH and EC were measured within 24 h ofextraction by methods outlined above. Zn, Cu, Pb andCd in pore water samples were analysed by ICP-MS.Dissolved organic carbon was measured as describedfor water extracts.

3 Results

3.1 Properties of the Materials

Some physico-chemical properties of the soils andbiosolids used are presented in Table 1. The pH of theWallaroo, Mawson Lakes and Bribie Island soils was8.4, 7.0 and 4.0, respectively, confirming them asalkaline, neutral and acidic. The soils are thereforereferred to as alkaline, neutral and acidic in Tables 2and 3 and Figs. 3, 4, 5 and 6. Both organic C andsoluble C content were greatest for the Mawson Lakessoil and least for the Wallaroo soil. Soluble Caccounted for 0.023–0.035% of the total organic Ccontent of the soils. EC was greatest for the MawsonLakes soil. Particle size analysis revealed that all threesoils were dominated by sand-sized particles but theyvaried greatly in clay content from 26% for theMawson Lakes soil to only 3% for the Bribie Islandone. Whilst BET surface areas were 11.9, 38.0 and0.21 m2 g−1 for the Wallaroo, Mawson Lakes andBribie Island soils, respectively, (Table 1) after 1-monthincubation with biosolids at a rate of 30 gkg−1, wemeasured values of 13.4, 48.1 and 0.33 m2 g−1 (datanot shown). Total contents of K, P, Cu, Zn, Pb and Cdwere least for the Bribie Island soil, intermediate for theWallaroo and greatest for the Mawson Lakes soil.

The biosolids used had a pH of 7.4, an organic Ccontent of 18.8% and a very high soluble organic C

Water Air Soil Pollut (2011) 221:351–363 353

content (Table 1). Soluble C accounted for 5.74% oftotal organic C content. Ash content was 53% (datanot shown). In South Australia, permissible metallevels in biosolids for land application are: Cu=200–750, Zn=250–1,400, Cd=3–11 and Pb=200–300 mg kg−1 so that the biosolids used in this studymay be suitable for land application after takingconsideration of total metal loadings per annum (EPA

South Australia 2009). However, regulatory metallimits vary greatly between states and countries and inthe Australian states of Queensland and New SouthWales, both Cu and Zn concentrations would beconsidered high (i.e. >375 and 700 mg kg−1 respec-tively) and indeed, Cu would be above regulatoryvalues in Canada, Sweden and Netherlands, Cd in theNetherlands, and Pb in Denmark (Epstein 2003). In

Table 1 Some physicochemical properties of the soils and biosolid used in studies

Parameter Soils/location Biosolid

Wallaroo, SA Mawson Lakes, SA Bribie Island, QLD Bolivar SA Water

pHw (1:5) 8.37±0.01 7.01±0.02 4.04±0.05 7.35±0.02

Organic carbon (%) 1.0±0.00 3.7±0.01 2.1±0.01 18.8±0.8

DOC (mg L−1) 0.47±0.01 1.8±0.05 1.5±0.01 2,160±90

EC (dS m−1) 0.57±0.03 1.32±0.01 0.14±0.01 8.3±0.3

%Clay 14±0.01 26±0.02 3±0.001 –

%Silt 16±0.01 23±0.02 2±0.001 –

%Sand 70±0.03 61±0.03 95±0.05 –

CEC (cmolckg−1) 7.7±0.80 21.3±0.40 2.2±0.20 –

BET surface area (m2 g−1) 11.9±0.0003 38.0±0.001 0.21±0.0001 –

Total (aqua regia) elemental concentration (mg kg−1)

K 1,890±60 2,420±50 150±15 3,900±200

P 96±4 120±6 21±3 26,000±1,000

Cu 17.34±0.5 21.53±0.4 0.90±0.03 680±30

Zn 17.09±0.20 67.75±2 3.22±0.2 750±30

Cd 0.12±0.00 0.35±0.00 0.05±0.00 1.40±0.07

Pb 8.2±0.2 37±2 0.8±0.1 67±5

Values are means±standard error (n=3)

Table 2 Percentage reduction in solution concentrations of Cu and Zn (compared to time 0) after 170 days incubation and change inpH at 170 days (compared to control at 170 days) in the biosolids-amended soils

Soil type Biosolids rate(g kg−1)

Cu (% reduction compared to time 0) Zn (% reduction compared to time 0) pH (unit changecompared to control)

Alkaline 10 49 b 78 c −0.2820 42 a 64 b −0.3330 40 a 50 a −0.33

Neutral 10 57 a 82 a −0.0120 56 a 76 a −0.0330 63 a 82 a −0.03

Acidic 10 7 a 0 a +0.13

20 33 b 28 b +0.26

30 52 c 36 c +0.35

Means within the same column and soil type followed by the same letter are not significantly different at P≤0.05 using Tukey’s test


general, concentrations of Cu, Zn and Pb in thebiosolids used could be considered elevated, but notexcessively high and those of Cd moderate. Becauseof similarities in their interaction with soil colloids,concentrations of all four of these metals in solutionwere determined during the incubation study.

Buffer curves for the three unamended andbiosolids-amended soils, and biosolids alone, areshown in Fig. 1a. These curves indicate the ability

of the material to resist changes in pH upon theaddition of OH− or H+ ions. The closer to thehorizontal the curve is, the greater the ability tobuffer pH and it is therefore evident that biosolids hada very high buffer capacity (Fig. 1a). Indeed, the pHbuffer capacity as, calculated from the curves (for achange in pH from 6 TO 7) was 120 mmol H+ orOH− kg−1 for biosolids and only 15 mmol H+ orOH− kg−1 for the acid soil. It is evident (Fig. 1a) thataddition of biosolids to each soil increased its abilityto mitigate acid and alkaline additions at the extremeends of the curves.

The effects of pH on the concentrations ofdissolved organic C, Cu, Zn, Cd and Pb in solutionin equilibrium with the biosolids sample over the pHrange 5.1–8.9 are shown in Figs. 1b and 2. Therelationships between solution pH and dissolvedorganic C, soluble Cu, Zn, Cd and Pb were fitted tolinear, quadratic and cubic regression functions.Quadratic functions gave the best fits for all relation-ships and regression equations and lines of best fit areshown in Figs. 1b and 2. Dissolved organic C andconcentrations of solution Cu and Pb increasedcurvilinearly with increasing pH while those of Zndecreased curvilinearly. There was a parabolic rela-tionship between pH and solution Cd (Fig. 2) sinceconcentrations were least at about pH 7.0 andincreased with both decreasing and increasing pH.

3.2 EC, pH and Dissolved Organic C in Pore Water

EC, pH and dissolved organic C in soil solution overthe 170-day incubation are shown in Fig. 3. Withincreasing rates of biosolids, EC was increased. Thiswas most obvious for the acidic soil (which had thelowest initial EC) but was also evident in the neutraland in the alkaline soil (except there was little

0

2

4

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8

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12

-120 -100 -80 -60 -40 -20 0 20 40 60 80 100 120mmol H/OH kg -1

pH

biosolid

alk 0

alk 30

neut 0

neut 30

acid 0

acid 30

y = 50.67x2 - 288.7x + 3819.R≤ = 0.98

3500

4000

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Dis

solv

ed o

rgan

ic C

(m

g L

-1)

Solution pH

a

b

Fig. 1 a pH buffering curves for biosolids and biosolids-amended soils; b effect of equilibrium pH on concentrations ofdissolved organic C in biosolids extracts

Property Metal Alkaline soil Neutral soil Acidic soil

Dissolved organic C Cu 0.64*** 0.82*** 0.73***

Zn 0.85*** 0.83*** 0.73***

Pb 0.18* 0.51*** 0.07 ns

Cd 0.46*** 0.71*** 0.13*

Solution pH Cu −0.14* −0.01 ns 0.25**

Zn −0.12* −0.24** 0.25**

Pb −0.26** −0.37*** −0.18**Cd −0.10* −0.25** −0.08 ns

Table 3 Correlation coeffi-cients (R2) and significanceof correlation between Cu,Zn, Pb and Cd concentra-tions in solution anddissolved organic C andsolution pH for the alkaline,neutral and acidic soils

Significance of correlationsshown: ns not significant

*P≤0.05, **P≤0.01,***P≤0.001


difference between the 20 and 30 gkg−1 rates for thealkaline soil). For all the soils, there was a tendencyfor solution EC to increase in the period up to 20 daysbefore declining and then more-or-less stabilising.

Over the entire incubation period, addition ofbiosolids resulted in a decrease in solution pH forthe alkaline soil but to an increase in pH for the acidicsoil (Fig. 3). For the neutral soil, biosolids additionsinitially tended to lower solution pH but by 140- and170-day incubation, there were no measureabledifferences in pH between treatments. In the alkalineand neutral soils, solution pH tended to increaseinitially but then decline again between 2 and 20 days.This decline in pH coincided with the peak in solublesalts during the same period suggesting a salt effectwas responsible. Thereafter, values increased up until80 days before tending to decline again. For the acidicsoil, pH increased during the first 50 days beforestabilising. Values for pH in pore water at time 0 inthe unamended soils were significantly less than thosein the 1:5 soil/water extracts (i.e. 7.3, 6.6 and 3.2compared to 8.4, 7.0 and 4.0, respectively, for thealkaline, neutral and acidic soils, respectively) reflect-ing a salt effect in soil solution which is diluted in a1:5 soil/water extract.

Dissolved organic C was increased with increasingadditions of biosolids and this effect was most

obvious in the alkaline and acidic soils. For theneutral soil, soluble organic C in all treatmentsshowed an exponential decline with increasing incu-bation time (Fig. 3). However, for the alkaline andacidic soils, there was a tendency for dissolvedorganic C to increase over the initial period of 2–20 days before declining rapidly between 20 and50 days of incubation. Concentrations of dissolvedorganic C were lowest in the neutral soil and similarin magnitude in the acidic and alkaline soils.

3.3 Concentrations of Cu, Zn, Cd and Pb in PoreWater

For the alkaline soil, solution Cu increased withincreasing rate of biosolids addition (Fig. 4). This trendwas less clear for Zn and only at the 30 gkg−1 biosolidsrate for Cd. At time 0, concentrations of solution Pbwere elevated by biosolids additions. Concentrations ofCu and Zn declined progressively over the incubation;the decline was more pronounced for Zn than Cu.There was also a decline in solution Cd and Pb duringthe first 4 days although additional peaks were evidentat 20 days for Cd and 35 days for Pb.

In the neutral soil, concentrations of solution Cuincreased with increasing rates of biosolids (Fig. 5). Asimilar trend was evident for solution Zn and Cd,

y = 438.0x2 - 4980.x + 17646R2 = 0.94

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3000

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6000

7000

8000

9000

4.0 5.0 6.0 7.0 8.0 9.0 10.0

So

luti

on

Cu

(μg

L-1

)

Solution pH

y = 90.91x2 - 1419.x + 5892.R2 = 0.94

300

400

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600

700

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luti

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Zn

(μg

L-1

)

Solution pH

4.0 5.0 6.0 7.0 8.0 9.0 10.0

y = 0.93x2 - 12.69x + 47.60R2 = 0.92

3

4

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6

7

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9

So

luti

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Cd

(μg

L-1

)

y = 13.62x2 - 155.8x + 490.6R2 = 0.98

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So

luti

on

Pb

(μg

L-1

)

Solution pH

4.0 5.0 6.0 7.0 8.0 9.0 10.0

Solution pH

Fig. 2 Effect of equilibrium pH on concentrations of soluble Cu, Zn, Cd and Pb in biosolids extracts


particularly at the 30 gkg−1 rate of biosolids, but forPb no such trend was discernible except at time 0. Inbiosolids-amended soils, concentrations of Cu, Zn, Cdand Pb declined with increasing incubation period.The decline was most pronounced during the initial20 days of incubation for Cu and the initial 4–10 daysfor Zn, Pb and to a lesser extent Cd.

For the acidic soil, solution Cu increased withincreasing additions of biosolids and this effect wasmost evident during the first 50 days of incubation(Fig. 6). For solution Zn, concentrations wereincreased progressively by increasing rates of bio-solids up to 20 gkg−1 but were similar at the 20 and30 gkg−1 rates. There was a tendency for Cdconcentrations to be increased by the two highest

rates of biosolids but for Pb no such trend was evidentexcept at time 0. At the two highest rates of biosolidsaddition, concentrations of solution Cu and Zngenerally declined over the incubation period. Asimilar trend was evident for solution Cd and Pbduring the first 30 days.

Concentrations of solution Cu and Zn were least inthe neutral soil (c.f. Figs. 4, 5 and 6). Concentrationsof solution Cu were similar in magnitude in the acidand alkaline soils but concentrations of solution Znwere markedly higher in the acidic soil. Concentra-tions of solution Pb were highest in the acidic soil andthose for Cd were least in the alkaline soil.

The degree of attenuation of biosolids-bornemetals was calculated by comparing the concentra-

1.5

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il so

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(d

S m

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Incubation time (days)

Alkaline soil

7.5

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Neutral soil

0.00.51.01.52.02.53.03.54.04.55.0

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il so

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(d

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Acidic soil

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Alkaline soil

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Incubation time (days)-acid soil

Acidic soil

Fig. 3 Changes in solution (a) EC, (b) pH and (c) dissolved organic C in pore water in three biosolids-amended soils of contrastingpH (alkaline, neutral and acidic) during a 170-day incubation period


0

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Cu

in

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(μg

/L) 0 g/kg 10 g/kg

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in s

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μg/L

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in

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il so

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(μg

/L)

Incubation time (days) Incubation time (days)


0.0

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Pb

in

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il so

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(μg

/L)

Fig. 5 Changes in Cu, Zn, Cd and Pb concentrations in pore water in a biosolids-amended neutral soil during a 170-day incubationperiod. Standard errors of the means shown

0

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in

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(μg

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)0.0

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Fig. 4 Changes in Cu, Zn, Cd and Pb concentrations in pore water in a biosolids-amended alkaline soil during a 170-day incubationperiod. Standard errors of the means shown


tions of metals in pore water at time 0 with thosepresent at 170 days and calculating the percentagereduction (Table 2). Because of the low concentra-tions present, this was not practicable for Cd and Pbbut results for Cu and Zn are shown in Table 2. In thealkaline soil, percentage reduction in solution Cu andZn decreased with increasing biosolids rate whilst inthe reverse was the case for the acidic soil. When pHvalues at day 170 are compared with control (Table 2),it is clear biosolids addition decreased solution pH inthe alkaline soil and increased it in the acid one (c.f.Figs 4 and 6).

3.4 Relationship Between Pore Water Characteristics

The relationships between solution pH or soluble Cand solution Cu, Zn, Cd and Pb were fitted to linear,quadratic and cubic regression functions. Linearfunctions gave the best fits for all relationships andcorresponding correlation coefficients are reported inTable 3. Concentrations of solution Cu and Zn in eachof the three soils were closely related to dissolvedorganic C concentrations and correlation coefficientswere highly significant (Table 3). Correlation coef-ficients between dissolved organic C and solution Pb

in the neutral soil and solution Cd in the alkaline andneutral soils were also highly significant. Except inthe acidic soil, all correlation coefficients betweensolution Cu, Zn, Pb and Cd and pH were negativealthough in most cases they were not highly signi-ficant. In the acidic soil, there was a significantpositive correlation (P≤0.01) between solution Cuand Zn and solution pH.

4 Discussion

The inorganic component of biosolids (53%) consistsmainly of oxides Si, Al and Fe (Sommers 1977;Jaynes and Zartman 2005) whilst the partly humifiedorganic component originates from human faeces(primary sludge) and bacterial cells (secondarysludge). Both components have the ability to immo-bilise heavy metals cations; the Al and Fe oxides byspecific adsorption and the organic matter by com-plexation reactions (Haynes et al. 2009). As a result,much of the heavy metal load in biosolids is bound tothe solid phase. The contrasting patterns of metalsolubility observed, as a function of pH, for biosolids-borne Cu, Zn, Pb and Cd (Fig. 1a) can be explained in

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Fig. 6 Changes in Cu, Zn, Cd and Pb concentrations in pore water in a biosolids-amended acidic soil during a 170-day incubationperiod. Standard errors of the means shown


relation to two main interacting factors. Firstly, withincreasing pH the charge on the surfaces of ampho-teric metal oxide materials and solid-phase organicmatter becomes increasingly negative thus favouringspecific adsorption of metal cations to the surfaces(McBride 2000). In addition, increasing pH favourssurface and bulk precipitation of metals as insolublemetal hydroxides (McBride 2000). Conversely,decreasing pH favours metal desorption as well asdissolution of precipitated metals and, as a result,metal solubility decreases with increasing pH.Secondly, with increasing pH the solubility oforganic matter increases and complexation of metalswith the dissolved organic matter tends to maintainor increase metal concentrations in solution (Bolanet al. 2011). Not only is there an increase in organicmatter solubility (Fig. 1b) but the forms of organicmatter present in solution change. For example, withincreasing pH there is an increasing proportion oflarge humic molecules present (Kipton et al. 1992;Bertoncini et al. 2005) and such molecules havesubstantial metal complexing ability.

For a metal such as Zn, which is present inbiosolids in substantive amounts in exchangeableform (Haynes et al. 2009), and has a relatively lowaffinity for organic matter (Stevenson 1994), increas-ing pH causes a decrease in solubility due toadsorption/precipitation reactions. The generalisedorder of affinity of metals for organic matter is Pb>Cu>Cd>Zn (Stevenson 1994) and for Pb and Cu theeffect of formation of soluble organic complexes withincreasing pH predominates and their solubilityincreases. For Cd, solubility decreased to a minimumat about pH 7 (presumably due to adsorption/precipitation), but thereafter it increased suggestingformation of soluble organo-Cd complexes at high pHvalues. Such marked effects on increasing metalsolubility with increasing pH (i.e. for Pb, Cu andCd) are less likely to occur in soils than in biosolidsalone due to the much lower organic C and, moreparticularly, soluble C contents in soils (see Table 1).Nonetheless, Ashworth and Alloway (2008) did noteincreases in the solubility of organic matter, Pb andCu above pH 6.5 in biosolids-amended soils.

As shown here, the water soluble “labile” organiccomponent in biosolids (which made up about 5.7%of total organic C content) can substantially elevatedissolved organic C concentrations in soil solution inbiosolids-amended soils. This component typically

contains sugars, aliphatic organic acids, amino acidsand soluble low molecular weight phenolic humicsubstances (Garcia et al. 1991). Concentrations insolution depend greatly on a balance between micro-bial production and degradation. For example, theincreases in concentrations of dissolved organicmatter present in soil solution during the first 3–20 days of incubation recorded (compared to time 0)in the biosolids-amended alkaline and acidic soilscould have occurred due to microbial degradation ofcomplex insoluble organic molecules in the biosolidswith the release of soluble material and/or excretionof organic metabolites by the microbial communitydecomposing the organic component of the biosolids.Thereafter, the concentration of dissolved organic Cdeclined. Several mechanisms may have contributedto this decline including its adsorption onto thesurfaces of soil Al and Fe hydrous oxides andprecipitation due to coagulation in the presence ofmultivalent ions (Haynes 2005) but the main processis likely to have been microbial decomposition. Thatis, dissolved organic matter is considered the mostdynamic C fraction in soils and it represents a majorsource of energy and cellular C for microbial activity(Bolan et al. 2011).

Although the Bolivar Wastewater Treatment Workscatchment includes a large industrial estate, concen-trations of heavy metals were not excessively high inthe biosolids attesting to effective pretreatment ofcontaminated industrial wastewaters prior to dis-charge into the sewage system. As already noted,metals may be present in biosolids in mobileexchangeable fractions as well as being bound toboth inorganic (e.g. Al and Fe oxides) and organic(e.g. humic) components. Indeed, controversy sur-rounds the relative importance of the properties ofbiosolids versus soil in governing biosolids-bornemetal solubility/bioavailability in biosolids-amendedsoils. It is generally assumed that biosolids propertiesdominate metal bioavailability in the short andmedium term but with time (over a period of years),biosolids properties have progressively less influenceand soil properties ultimately control availability(Smith 1996). However as shown in this study, soilproperties can have a significant influence in the firstfew weeks and months following biosolids applica-tion. Indeed, both biosolids and soil properties will beimportant since both materials contain inorganic andorganic colloids with the capacity to adsorb/complex


heavy metals. For example, the strong affinity of Pbfor the surfaces of soil colloids is demonstrated by thefact that although biosolids additions to all soilsincreased solution Pb concentrations at time 0, con-centrations very rapidly decreased to low levels. Onthe other hand, the influence of biosolids on soilproperties was evident in that BET surface area wasgreater in biosolids-amended than unamended soils.

Because of its neutral pH and large bufferingcapacity, addition of biosolids increased the pH of theacid soil and decreased that of the alkaline one.However, it is not only the pH and buffering capacitybut also the high soluble salts content of biosolids thataffects soil pH. That is, the immediate accumulationof exchangeable cations (e.g. Ca2+, Mg2+, K+ andNa+) in solution, originating from the biosolids, willdisplace H+ and Al3+ from exchange sites therebyincreasing their concentration in soil solution andlowering solution pH. Similarly, following rewettingof an air-dried soil there is a flush of N mineralizationand an accumulation of NO3

− and associated cationsin solution. Thus, there was an initial increase in ECin solution in both the control and biosolids-treatedsoils (particularly for the alkaline and neutral soils).This was associated with a decline in solution pH. Asthe accumulated cations equilibrated with the cationexchange sites of the soil, cation concentrations insolution declined and solution pH rose again.

The negative correlations between solution pH andCu, Zn, Pb and Cd solubility for the alkaline andneutral soils were expected since, as already dis-cussed, with increasing pH the solubility and avail-ability of these metal cations characteristicallydecreases (Sparks 2003) due to high pH favouringadsorption/precipitation reactions. In the case of thesetwo soils, increasing additions of biosolids reduced orhad little effect on pH while, at the same time,increasing metal loading to the soil. Both factorsfavour an increase in concentrations of metals insolution thus leading to the negative correlations. Bycontrast, for the acidic soil, there was an unexpectedpositive correlation between Cu and Zn solubility andsolution pH. This is attributable to increasing bio-solids application rates increasing both the loadingrate of metals to the soil as well as solution pH.However, the soil had a very low initial pH (4.0) andeven at the 30 gkg−1 biosolids rate, solution pH wasraised to only 4.7. At such a pH value, metal cationswill still be reasonably soluble. Thus, increasing pH

was of less significance than the increasing loadingrate and as a result, solution metal concentrationsincreased.

The positive correlation between concentrations ofdissolved organic C and solution Cu, Zn, Pb and Cdis explicable in terms of increasing additions ofbiosolids causing increases in both metal loadingand concentrations of soluble organic matter present.In addition, a substantial proportion of the metalspresent in solution may well have been complexedwith the soluble organic matter. Indeed, a majorcontributor to heavy metal mobility in biosolids-amended soils is thought to be the formation ofcomplexes with dissolved organic matter releasedfrom the biosolids (Lamy et al. 1993; McBride et al.1997, 1999). The dissolved organic matter acts as a“carrier” for heavy metals and elevated concentrationsof both heavy metals and dissolved organic matter arefrequently found together in leachates from biosolids-treated soils (Toribio and Romanya 2006; Antoniadiset al. 2007). Even for metals such as Zn and Cd,which are traditionally assumed to complex onlyweakly with soluble organics, a substantial proportion(i.e. >50%) of the soluble fraction can be present incomplexed form (McBride et al. 1999; Li et al. 2001;Schwab et al. 2007). Thus, the positive correlationsreflect the importance of biosolids-derived solubleorganic matter in affecting heavy metal solubility inbiosolids-amended soils.

Significant attenuation of metals in the acidicBribie Island soil was surprising considering its lowpH (4.0), low clay content and low BET surface area.Certainly, the most substantial increases in soluble Cuand Zn with increasing biosolids applications oc-curred in this soil. Indeed, it is evident (Table 2) thatthe percentage reduction in solution Cu and Zn(between 0 and 170 days) was negligible at thelowest biosolids rate and increased with increasingrates as solution pH rose. By contrast, for the alkalinesoil, the percentage reduction in Cu and Zn solubilityactually decreased with increasing biosolids rates.However, in this case biosolids applications tended tolower pH and therefore promote metal solubility.These data therefore confirm the assertions of othersregarding the importance of raising soil pH in order toachieve effective metal attenuation in soils (Allowayand Jackson 1991). Nonetheless, the greatest percent-age attenuation, at each rate of biosolids addition,occurred in the neutral Mawson Lakes soil. This soil


did, however, have the greatest clay and organicmatter contents and the highest BET surface area. Ittherefore had the greatest capacity to adsorb metals toits surfaces thus lowering concentrations in soilsolution.

5 Conclusions

The solubility of biosolids-borne metals in soils in thefirst 6 months after application can be influencedsubstantially by the properties of the soil as well asthose of the biosolids. Solution pH, dissolved organicC and the intrinsic capacity of the soil to removemetals from solution (i.e. clay and organic mattercontent and BET surface area) were found to be themain factors interacting to regulate metal solubility inbiosolids-amended soils. A period of a few monthsageing in biosolids-amended soils can lead to sub-stantial reductions in heavy metal cation solubilityand potential phytotoxicity.

Acknowledgements The first author thanks the HigherEducation Commission (HEC) of Pakistan for funding of hisPost-Doctoral position. We are also grateful to the University ofSouth Australia and CRC CARE for providing facilities for thisresearch.

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Natural Attenuation of Zn, Cu, Pb and Cd in Three Biosolids-Amended Soils of Contrasting pH Measured...

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