Journulr?

fSoilScience, 1993,44,97-110

Effects of time and temperature on the bioavailability

of Cd and Pb from sludge-amended soils
P. S. H O O D A & B. .I.
ALLOWAY
Environmental Science Unit, Geography Department, Queen Mary & Westfield College,
University of London, Mile End Road, London El 4NS, U K

SUMMARY
A pot experiment was conducted to compare the behaviour and bioavailability of Cd and
Pb from two soils mixed with sewage sludge at three rates (0, 50 and 150 t ha-') and
maintained at two contrasting ambient temperatures (15C and 25C) over a period of one
year following the treatments. Ryegrass (Lolium perenne) accumulated Cd and Pb in the
sewage sludge treated soils, although accumulation was significantly lower in the soils
treated at the high rate (1 50 t ha- I ) compared to the low rate (50 t ha - I ) . Ryegrass grown
in the warm environment (25C) accumulated significantly higher levels of Cd and Pb than
that grown in cooler conditions (1 5OC). Samples of the soils spiked with nitrate salts of Cd
and P b a t equivalent rates of metal loading resulted in the ryegrass accumulating much
higher levels of both the metals than on the sludge treated soils.
Metal uptake by the ryegrass from the sludge treatments increased over successive
harvests while that from metal salt treatments decreased. The observed trend of increasing
plant metal uptake over time coincided with a trend of decreasing pH in the sludge
treatments. However, the concentrations of Cd and Pb extracted by DTPA failed to
predict the changes in plant metal uptake. The importance of sewage sludge as both a
source and a sink of pollutant metals and the trend of increasing bioavailability over time
shown by this experiment are discussed.

INTRODUCTION
The disposal of sewage sludge on agricultural land is increasing throughout the world. Although
sewage sludge contains agronomically useful amounts of N and P, and has valuable soil conditioning properties (Epstein, 1975; Chang et al., 1983), the concentrations of several potentially harmful
contaminants commonly found in sludges limit the extent to which they can be applied to land.
These contaminants include trace metals such as Cd, Cu, Cr, Ni, Pb and Zn and organic micropollutants such as polycyclic aromatic hydrocarbons and polychlorinated biphenyls. There is a
significant risk that some of these contaminants will affect human health by accumulation in food
crops. This is particularly important in the case of trace metals, such as Cd, which has a relatively
high bioavailability. Of the factors known to control the bioavailability of sludge-borne trace
metals, soil pH (Mahler et a/., 1980; Narwal et al., 1983; Eriksson, 1989; Alloway et a/., 1990;
Jackson & Alloway, 1991), concentration of sludge-borne metals (Rappaport et al., 1988), organic
matter (Maclean, 1976), and temperature appear to be most important.
Studies on the changes in the bioavailability of trace metals with time have generally shown that
anomalously high concentrations of many metals remain available for several years after the application of sludges (McGrath, 1987; Alloway & Jackson, 1991). Several authors found that metal
availability remained more o r less the same (Chang et a/., 1982; McGrath, 1987), whereas others
reported decreases after the last sludge application (Hinesly et al., 1979; Bidwell & Dowdy, 1987;
Morel et a/., 1988). Some authors reported increases in availability with time, at least for some

97

P.S . Hooda & B. J. Alloway

98

elements, such as M o (Soon & Bates, 1985) and Ni (Korcak & Fanning, 1985). De Haan (1975)
predicted that the availability of sludge-derived metals in most soils will eventually increase due to
acidification by nitrification and leaching. However, it is now the normal practice to maintain the
p H of sludged soils at around 6.5. Several workers have also reported that the bioavailability of
metals from soils spiked with metal salts is much greater than that of the equivalent amounts of
mctals in sludged soils (Mahler et al., 1980; Korcak & Fanning, 1985). This is an important
consideration because metal contamination from sewage sludge is often simulated by spiking with
metals.
The fate of metals added to soils in sewage sludges will depend upon the chemical processes
operative in the stabilization period after sludge application. It was therefore considered important
to study changes in soil chemical parameters during this period and to assess thcir influence on
bioavailability of the metals. The objectives of the investigations were: (i) to measure the changes
over a twelve month period in soil pH and organic matter in the different treatments; (ii) to follow
trends of bioaccumulation of Cd and Pb by ryegrass; (iii) to measure amounts of Cd and Pb
extracted by DTPA; (iv) to compare the bioaccumulation of equivalent concentrations of Cd and Pb
from sludged and metal-spiked soils; and (v) to assess the effects of markedly different ambient
tcmpcraturcs on the chemistry and bioavailability of added metals.
MATERIALS A N D METHODS
Soil treutments
Bulk samples of topsoil (0-1 5 cm) wcre collected from two sitcs on agricultural land in England and
thcir propcrties are shown in Table I . Onc was a sandy soil from a farm near Thetford in the
Breckland region of East Anglia. This was a brown sand of the Worlington/Methwold series
developed on decalcified glacial drift overlying chalk. The other soil was sandy loam of the
Bursledon series (gleyed brown earth) on drift over Eocene clay from a pasture near Brentwood in
Essex. The bulk samples of soil were air dried, sieved ( < 5 mm coarse nylon mesh) and thoroughly
homogenised. The soils were mixed with the appropriate amounts of sludge or metal salt solutions
and allowed to air dry before further grinding and sieving (<2 mm). 4.6 kg of air-dry soil mixture
was added to each PVC pot.
Table 1. Some physico-chemical properties of the soils and sludge
Variahlc

PH ( H P )
Organic matterJ (g kg
LOI"(g kg I)
Bulk dcnsity (kg m ')
CEC (cmol, kg I )
Sand (g kg I)
Silt (g kg I)
Clay (gkg 7
FIee Mn (pg g I )
Reducible Fc (pg g I)
Zil

cu
Pb
Ni
Cd

Sandy loam

I)

5.4
36. I
62.0
1.18
18.94
586
207
177
I18
I200
58.16
18.25
52.10
16.1 1
0.45

,'Determined by the method of Walkley & Black

"Loss on ignition at 400C.

Breckland sand

6.58
14.1
19.7
I .45
4.75
922
47
5
77
200
Total Metal (pg g
27.40
7.70
14.38
7.63
0.12

Sludge

5.92
_.

556.5
0.63
~

I)

1408
1031
706
259
40

Bioavailahility of Cd and Ph

99

A sample of anaerobically digested liquid sewage sludge was obtained from a sewage works in an
urban area and mixed with the two soils a t proportions equivalent to the following field application
rates: control (no sludge), 'low' sludge rate (50 t ha-') and a 'high' rate (150 t ha-'). Equivalent
amounts of Cd and Pb nitrate solutions were added to other samples of soil to give the same low and
high loadings of metals as in the sludge treatments. The resultant metal concentrations under the
different treatments are given in Table 2.
Table 2. Cadmium and lead concentration (pg g- I) in the soils resulting from sewage sludge
application and metal-salt spiking
Sandy loam
Treatment
Sewage sludge application
Control (0 t ha-')
Low sludge (50 t ha ')
High sludge (1 50 t ha I)
Metal-salt spiking
Low spiking
High spiking

Breckland sand

Cd

Pb

Cd

Pb

0.45
2.02
5.66

53.1
77.13
131.82

0.12
2.00
5.62

13.7
42.5
97.1

2.43
6.07

82.1
142.2

2.04
5.85

42.6
100.4

In ordcr to investigate the effects of temperature, triplicate pots of each treatment were placed in
a cool and a warm environment. The warm environment was provided in a greenhouse with the
ambicnt temperature controlled at 25 f3C but with daylight hours varying according to season.
For the cool environment, another set of triplicate pots were placed in a growth chamber where the
temperature was 15 & 2C with 12 h daylight.
Pot experiments
The pot experiments commenced in January 1990 and on the first day (Day 0) each pot was
saturated with deionised-distilled water and thereafter the pots were irrigated regularly in order to
keep the soil moist during the experiments. Pots in the warm environment normally required
irrigation twice a week but those in cool conditions needed irrigation only once a week. After an
equilibration period of 1 month, ryegrass was sown as a test crop to compare the bioavailability of
thc metals in different treatments. All experimental pots received a small startcr treatment of
powdered compound fertilizer supplying small amounts of N, P and K. The first cut of ryegrass was
made 6 weeks after sowing and thereafter the grass was cut at intervals of 4 weeks. The harvcstcd
ryegrass samples were washed with distilled water followed by a rinse in deionised-distilled water
before drying at 65C.
Composite soil samples were taken at a depth of 0-7.5 cm from all the treatments on days 1 , 15,
30,60, 120,240, and 360. These soil samples were air dried and passed through a 2-mm mesh prior to
analysis.

Soil analyses
The total concentrations of trace metals in soil and sludge samples (i
2 mm) were determined in
filtered extracts obtained from I -g samples of those materials which were digested in concentrated
hydrofluoric and perchloric acids (Tessier et al., 1979). All samples were prepared and analysed in
duplicate with reagent blanks. Subsamples of the certified reference materials, sludged soil BCR No.
143 and lake sediment IAEA SL-1, were used in all batches of samples analysed for quality control.
Trace metal concentrations in all final solutions were determined by flame atomic absorption
spcctrometry using an IL (Thermoelectron) S12 atomic absorption spectrophotometer with Smith
Hieftje background correction.

I00

P . S. Hooda & B. J. Alloway

The hydrous Mn oxide contents of the soils were determined after extraction of the soils with
hydroxylamine hydrochloride (Chao, 1972) and hydrous Fe oxide contents by extraction with
sodium dithionite (Avery & Bascomb, 1974). The soil parameters measured were: texture by the
pipette method (Day, 1965), pH in distilled water (1:2.5 w/v), bulk density (Avery & Bascomb,
1974), organic matter content, calcium carbonate equivalence and cation exchange capacity (Hesse,
1971). Data for thc soil and sludge physico-chemical parameters are presented in Table I . The soil
samples taken from all the treatments at regular intervals during the experiments were analysed for
pH, organic matter content and metals extracted by 0.005 M diethylenetriaminepentaaceticacid
(DTPA) (Lindsay & Norvell, 1978).
Plant analyses
For plant tissue analysis, only samples from the first, third, sixth and ninth harvests were analysed.
The washed and dried samples were finely ground and stored in acid-washed sample bottles.
Subsamples (0.5 g) of milled tissue wcrc digested in a concentrated HN0,-HCIO, (AristaR gradc,
BDH Chemicals) mixture prior to determination of Cd and Pb by atomic absorption spectrometry.
All of thc plant analyses were carried out in standard batch formats. Replicate anatyses of all the
samples were made together with reagent blanks and the certified reference materials (CRMs)
aquatic plant tissue BCR No. 60, olive leaves BCR No. 62 and tomato leaves NBS No. 1573 for
quality control. Thc observed C R M valucs were within the certified ranges of the metals. For Cd,
all the solutions were analysed first by flame atomic absorption spectrometry (FAAS), but those
with Cd concentrations below the detection limit of FAAS were subsequently analysed by electrothermal atomization atomic absorption spectrometry (ETAAS). The low concentrations of Pb in
the ryegrass samples necessitated that all Pb analysis be made by ETAAS.
Statistical analyses
Metal concentrations in plants and soils under different sewage sludge and metal salt spiking
treatments were evaluated by the least significant difference (LSD) test. Nearly all the interactions
were statistically significant a t PGO.01 or P<0.05.
RESULTS
Grass growth was slower in the cool environment compared to the warm environment. The higher
rate of sludge application enhanced ryegrass growth but in the spiked soil treatments ryegrass was
stunted and chlorotic. The chlorosis was most severe in the high rate of metal spiking where the
plants failed to tiller and had to be resown after every harvest.
The addition of sewage sludge to the soils increased the soil organic matter contents substantially
(Fig. I ) . Although thc organic matter contents decreased rapidly in the first 50 d aftcr mixing, they
showed only a very gradual decrease over the rest of the year and remained much higher than the
respective controls at the end of the period. A similar increase in soil organic matter content after
sludge application, followed by a 50% decline due to decomposition, was reported by Robertson
et al. (1982). Soil pH values were also affected by the sludge applications. In the sandy loam, the pH
incrcased from pH 5.4 to 6.8 initially, but decreased rapidly (Fig. 2) in the first 30 d and the pH of the
low sludge treatment decreased to less than that of the control after 100 d. After an initial slight
increasc, the p H of the Breckland sand decreased significantly below that of the control and
remained like this for the rest of the year (Fig. 2). Decreases in the pH of soils amended with sewage
sludge h a w been widely reported in the literature (Silviera & Sommers, 1977; Robertson et al.,
1982). All the soils spiked with metal salts showed decreased soil p H values in the early stages. A year
after spiking, the p H of Breckland sand was similar to its control whereas the pH of the spiked sandy
loam remained lower than that of its control.

Cadmium and lead accumulation in ryegrass

The mean concentrations of Cd and Pb in ryegrass grown in the different treatments are shown in
Tables 3 and 4, respectively. Differences in Cd and Pb in ryegrass in the various treatments werc
statistically significant. The addition of Cd and Pb to soils both as sewage sludge and as metal salts

Bioavailahility of Cd and Ph

101

4-1

resulted in substantial increases in the concentrations of these metals in the ryegrass tissue relative to
the controls. The amounts of both Cd and Pb accumulated in the plants on the spiked soils were
several timcs higher than those in the sludge-treated soils (Tables 3 and 4). Similar differences in Cd
and Zn accumulation in maize tissue were observed by Korcak & Fanning (1985) while invcstigating
metal accumulation from sludged and metal-spiked soils. As shown in Tables 3 and 4, the differences
in metal loadings between the high and low metal-spiked soils were closely reflected in the concentrations of the metals in the ryegrass. In contrast to the spiking treatments, the concentrations of
metals accumulated in the ryegrass on the sludge-treated soils were actually lower in the high sludge
trcatments (150 t ha-') than in the low sludge treatment (50 t ha-') in both cool and warm environments (Fig. 3). This could be due in part to a certain amount of dilution resulting from a slightly
increased growth of grass at the high rate of sludge. However, these findings would appear to
support the conclusions of Corey et al. (1987) that the sewage sludge matrix acts as a major
adsorptive tnedium for metals in sludged soils. The higher the amount of sludge applied, thc greater
the total adsorptive capacity of the soil for trace metals, at least in the short term. In the spiking
treatments, where no additional adsorptive material was added to the soils, the different adsorptive
capacitics of the soils themselves control the bioavailability of the metals. It is also important to note
that no significant differences were found between the accumulation of Cd in ryegrass on either the
sludge-treated Brcckland sand or the sandy loam (Table 3), but in the spiking treatments C d uptake
was significantly higher from the Breckland sand and Pb uptake greatest from the sandy loam
(Table 4). Hence the sandy loam with greater clay and hydrous Mn and Fe oxide contents gives rise

P.S . Hooda & B. J . Alloway

102

4 1
0

I00

200

30 0

I0

Residual period (d)

Fig. 2. Changes in soil pH resulting from sewage sludge application: (a) Breckland sand; (b) Sandy loam.
0 control, low sludge, A high sludge.

to a decrease in the availability of Cd and an increase in the availability of Pb relative to the

Breckland sand.
The ejjects of temperature on metal uptake
Thc data for Cd and Pb uptake by ryegrass when averaged over harvests, soils and treatments,
showed that the difference in temperature between the cool ( 1 5 2C) and the warm (25 f3C)
environments significantly increased ( P < 0.01) their accumulation in plant tissue (Tables 3 and 4).
The increment in uptake due to the increase in environmental temperature was slightly greater for
Cd (77%) than Pb (65%). Furthermore, the averaged data for all treatments showed that the
bioaccumulation of Cd in both the environments is higher on the Breckland sand than on the sandy
loam (Table 3). Conversely, the uptake of Pb was greater from the sandy loam soil (Table 4).
As shown in Tables 3 and 4, the increase in temperature enhanced accumulation of both the
metals by ryegrass in all treatments (including controls). However, the effect was more marked in
metal-spiked than sludged soils. In warm conditions, the lower metal uptake from the high sludge
treatment was not as pronounced as it was under cool conditions (Fig. 3). In a long-term field trial,
Chang et ul. (1987) found soil temperature to be one of the major factors accounting for the
variations in metal accumulation by crops.

The efiects oftime on metal uptake

The Cd uptake data from the sludge treatments showed that there was a reduction in Cd accumulation in the third harvest (Fig. 4). In contrast, Pb uptake shows a steady and significant increase

Bioavailability of Cd and Ph

103

Table 3. Mean uptake of cadmium (pg g- DW) by ryegrass grown on sludged and metal-salt spiked soils under
two growing environmentsd
1st Harvest

3rd Harvest

6th Harvest

9th Harvest

Treatmcn 1

Coal

Warm

Cool

Warm

Cool

Warm

Cool

Warm

Sandy loam soil

Control
Low sludge
High sludge
Low spiking
High spiking

0.33
0.86
0.60
2.41
9.40

0.74
1.68
1.47
3.78
15.11

0.25
0.70
0.55
3.43
7.09

0.53
2.50
2.81
3.84
12.59

0.25
0.99
0.87
3.54
7.87

0.45
2.65
2.75
4.35
13.78

0.23
1.08
1.05
3.55
7.52

0.39
2.88
2.76
4.37
14.21

Brcckland sand
Control
Low sludge
High sludge
Low spiking
High spiking

0.32
1.02
0.83
4.45
9.43

0.41
1.59
1.30
6.78
17.84

0.25
1.05
0.77
3.27
6.80

0.28
1.73
2.64
5.66
15.97

0.17
1.79
0.89
3.91
8.78

0.28
2.40
2.70
4.54
16.05

0.17
1.65
1.08
3.72
9.07

0.28
2.46
2.85
4.58
15.09

Cool and warm represent 15 & 2C and 25 3C ambient temperature, respectively.

hAllthe treatments and their interactions were significantly different at PG0.05.

Table 4. Mean uptake of lead (pg g I DW) by ryegrass grown on sludged and metal-salt spiked soils under two
growing environments
1st Harvest

3rd Harvest

6th Harvest

9th Harvest

Treatment

Cool

Warm

Cool

Warm

Cool

Warm

Cool

Warm

Sandy loam
Control
Low sludge
High sludge
Low spiking
High spiking

0.193
0.273
0.218
0.731
2.056

0.240
0.519
0.409
1.174
2.279

0.252
0.357
0.274
0.627
1.426

0.294
0.762
0.762
1.297
2.115

0.189
0.430
0.413
0.700
1.413

0.272
0.909
0.918
1.189
2.005

0.197
0.489
0.537
0.663
1.287

0.212
1.014
0.999
1.315
2.171

Breckland sand
Control
Low sludge
High sludgc
Low spiking
High spiking

0.092
0.170
0.120
0.652
1.603

0.128
0.348
0.315
0.957
1.924

0.101
0.192
0.097
0.464
1.424

0.166
0.347
0.365
1.144
1.861

0.098
0.253
0.232
0.473
1.315

0.176
0.435
0.456
1.332
1.804

0.107
0.364
0.251
0.540
1.360

0.202
0.420
0.454
1.277
2.006

All thc treatments and their interactions were significantly different at PG0.05

ovcr the successive harvests in relation to the first cut (Fig. 4). Although Cd accumulation data
showed a significant decrease (PgO.01) over time in the controls and metal-spiked treatments
(Table 3), Cd uptake from the sludge treatments increased over the residual period (Fig. 4). The rate
of increase in Cd uptake over the time period was greater from the high sludge treatment than the
low sludge treatment, but the concentrations of the metal were still lower from the high sludge
treatments. Nevertheless, the magnitude of difference in Cd uptake between high and low sludge
treatments was greater in the first cut than in subsequent cuts (Table 3).

P.S. Hooda & B. J,Alloway

104

s'
a

I50

-I

Ul

100

Y
a,

050

0 00
0.60 I
0

s'
a

50

040

IUl

030

Y
a,
Y

0.20

a
0.10
0.00
0

50

150

Sludge application rate (t ha-')

Fig. 3. Cadmium (a) and lead (b) uptake by ryegrass from the sludge-amended soils. W cool(loam), El warm(loam), n cool (sand), H warm(sand).

As shown in Table 4 and Fig. 4, Pb uptake increased over time from all the treatments, except the
high metal-spiked soils. It is important to recognise that the difference in the physiological age of the
ryegrass sampled from the high metal-spiked soil treatments may influence the comparison of plant
uptake data from different harvests on spiked and sludged treatments. As a result of resowing the
ryegrass due to the phytotoxic effects of the high metal spikes, the grass was physiologically young
while that on the other treatments was up to one year old. As with Cd, there was hardly any
difference in Pb uptake from the two sludge treatments in the cuts of ryegrass taken a year after the
application of the sewage sludge (Fig. 4). The results indicated that the accumulation of Cd and Pb
from the sludge treatments over the residual time period was still gradually increasing. Other
workers have also demonstrated the increased plant accumulation of sludge-borne metals with time
after sludge application (Schaurer et al., 1980;Narwal et al., 1983),but Chang et al. (1982,1987) and
Sanders et al. (1987) did not find this.
Accumulation ratios
The mean accumulation ratios for Cd and Pb in different treatments are given in Table 5. The
accumulation ratio is defined as the concentration of an element in plant tissue relative to its total
concentration in the soil. The accumulation ratios in the control treatments show Cd to be between
200 and 440 times more readily accumulated than Pb. In the sludge and metal-spiking treatments,
Cd tends to have accumulation ratios between 60 and 160 times greater than Pb. These higher
accumulation ratios indicate that Cd is much more likely to accumulate in the food crops grown on

Bioavailability of Cd and Ph
100

105

10

Residual period (harvests)

Fig. 4. A comparison of Cd (a) and Pb (b) uptake by ryegrass from sandy soil amended with sludge and spiked
- x - low sludge, -Alow salt, -0- high sludge, -A- high salt.
with metal salts. --n-control,

contaminated soils than Pb. The accumulation ratios clearly show that the relative uptake of the
metals decreases with sludge application rate. At the high sludge rate (150 t ha-') the accumulation
ratio for Cd is 4 times lower than that for the low sludge application rate (50 t ha-'), whereas for Pb
the factor is little over 2 (Table 5). Accumulation ratios for the Cd and Pb treatments in the warm
environmcnt are around twice as high as those in the cool environment.
D T P A extractability
Partial extractions with the chelating agent DTPA have been used by many workers as a prediction
of the amounts of metals which are bioavailable. The data in Tables 6 and 7 show that the concentrations of DTPA-extractable Cd and Pb increased markedly as a result of the addition of the metals
in both sewage sludge and metal spikes. However, DTPA-extractable Cd and Pb concentrations
were more than twice as high in the metal salt-spiked soils compared to the equivalent sludged soils.
Increased extraction of metals by DTPA with increasing rate of sewage sludge or metal salt additions
is well documented in the literature (Schauer et al., 1980; Korcak & Fanning, 1985; Rappaport et al.,
1988). DTPA extraction data from all the periodic samplings, averaged over treatments, showed
that both the Cd and Pb were extracted in higher amounts from the sandy loam soil than from the
Breckland sand (Tables 6 and 7). DTPA-extractable concentrations of Cd and Pb from all the
treatments in the cool environment were slightly higher than those from the warm environment.
Howevcr, the effects of temperature on metal extractability were not clear when compared within a

106

P.S. Hooda & B. J. Allowuy

Table 5. Mean bioaccumulation ratios of Cd and Pb from different
sludge and metal-spikingtreatments"

Sandy loam
Treatment

Breckland sand

Cd

Pb

Cd

Pb

0.73
0.42
0.10
0.99
1.55

0.0036
0.0035
0.0016
0.0089
0.0144

2.66
0.52
0.14
2.18
1.59

0.006
0.004
0.001
0.015
0.016

1.62
0.82
0.26
1.56
2.49

0.0045
0.0067
0.0031
0.0143
0.0160

3.25
1.26
0.23
3.32
3.04

0.0093
0.0081
0.0032
0.0227
0.0191

Cool environment

Control
Low sludge
High sludge
Low spiking
High spiking
Warm environment

Control
Low sludge
High sludge
Low spiking
High spiking

~~

;'Mean bioaccumulation ratio is the ratio of plant conccntration

o f a n element to its total concentration in the soil.
trcaimcnt o r for one of the soils. Thcre were no significant changes in DTPA-cxtractable Cd ovcr thc
rcsidual period (Table 6) which departs from the trend of the data for Cd uptake by ryegrass. DTPAcxtractablc Pb showcd a significant decreasc (P,<O.OI) over the year from the commcnccmcnt of thc
expcrimcnt (Table 7 ) whereas data for Pb uptake by ryegrass showed a significant increase. Likewise,
the plant uptake data showed consistently higher concentrations of both Cd and Pb in the warm
environment compared to the cool but thc DTPA data did not rcflect this at all. Thcrcfore it must bc
concludcd from the results obtained in this pot experiment that DTPA did not enable the obscrved
trcnds in plant metal uptake to be prcdicted.
DISCUSSION
Four major findings have emerged from this work; these are (i) the importance of the sewage sludge
matrix as an adsorptive mcdium for the metals, (ii) the increased uptake of metals by plants under
higher temperature conditions, (iii) the decrease in pH of sludge-treated soils in the residual period,
and (iv) thc trend towards increased uptakeofCd and Pb in the long term during the residual pcriod.
The fact that sewage sludge acts both as a source of trace metals and also as a major adsorbent
for them is very important. It has been pointed out by Corey et a/. (1987) that, at high rates of
application, the sewage sludge itself becomes the major factor determining the bioavailability of
sludgc-bornc metals rather than the physico-chemical properties of the soil. However, it has been
shown in this experiment that the changes occurring in the physico-chemical propertics of the
sludge-soil mixture after the cessation of sludge applications are of paramount importance in
determining the bioavailability of metals and nced to be considered when formulating a long-term
policy for sewage sludge disposal. In the light of predicted changes in climate over the next few
decades, thc cffcct of temperature on thc bioavailability of contaminant metals in sludge-amendcd
soils is likely to be highly significant. It should be mentioned that Keefer et a/. (1 986) did not find a
significant effect of sludge application rate on metal uptake but many other workers have reported
increased uptake of metals with increased rate of sludgc application (Heckmanet al., 1987; Chang et
a/., 1987), but all these refer to field experiments rather than pot experiments.
Thc DTPA cxtraction data showed that extraction of the metals from metal salt-spiked treatments was 2-3 times more than the extraction from equivalent sludge treatments and this correlated
closely with the accumulation of metals from the two types of treatment. However, thc lack of

2.34
5.98

2.42
6.20

0.06
0.89
2.08
1.74
5.06

Low spiking
High spiking

Breckland sand
Control
Low sludge
High sludge
Low spiking
High spiking

0.06
0.85
2.13
1.68
5.11

2.14
6.01

0.18
0.94
2.25

0.05
0.73
1.85
1.67
4.99

2.28
5.97

0.18
1.10
2.25

Day 15

0.06
0.79
2.17
1.69
5.05

2.39
6.23

0.18
1.11
2.58

0.06
0.81
2.10
1.68
4.99

2.19
5.85

0.18
1.06
2.43

Day 30

0.06
0.81
2.11
1.61
4.83

2.32
6.39

0.19
1.20
2.59

0.06
0.91
2.22
1.64
5.05

2.26
6.20

0.19
1.10
2.71

Day 60

0.05
0.70
1.93
1.65
5.02

2.24
6.36

0.18
1.02
2.40

0.06
0.74
2.23
1.17
4.97

2.01
6.12

0.18
1.06
2.24

Day 120

0.06
0.98
2.22
1.69
4.79

2.40
6.37

0.18
1.14
2.40

0.06
0.81
2.23
1.59
4.83

0.18
1.21
2.77
2.32
6.08

Day 240

"C and W represent cool (1 5 & 2C) and warm (25 3C) growing environments, respectively.
bAllthe treatments except time, temperature x time, temperature x treatment and time x treatment were significantly different at P< 0.05.

0.05
0.90
1.88
1.76
5.03

0.17
0.96
2.20

0.18
0.94
2.28

Sandy loam
Control
Low sludge
High sludge

Treatmentb

Day 1

0.06
0.99
2.31
1.64
4.94

0.06
0.82
2.10
1.56
5.03

2.16
2.18
5.90

2.44
2.36
6.26

w
0.19
1.41

Day 360

0.20
1.31

Table 6. Changes in DTPA-extractable Cd (pg g-') as affected by sludge application and metal-salt spiking under two ambient temperatures"

2n

=:
c

5
-.

Tf?.

12.0
16.3

29.8
39.1
67.0

1.1
11.6
27.0
20.5
66.2

Sandy loam
Control
Low sludge

High sludge
Low spiking
High spiking

Breckland sand
Control
Low sludge
High sludge
Low spiking
High spiking

1.2
12.4
26.5
20.5
65.3

29.3
37.9
65.9

12.4
16.9

1.1
10.6
26.4
18.3
59.5

29.1
37.6
67.3

12.9
16.2

1.1
10.3
22.3
18.3
56.1

26.2
35.7
64.6

11.7
18.4

Day 15

1.2
9.0
28.1
18.1
57.6

30.6
38.0
59.0

13.7
18.3

1.2
10.7
23.5
15.6
54.1

27.7
35.7
62.1

13.2
17.6

Day 30

"All the treatments and their interactions were significantly different at P < 0.05

Treatment"

Day 1

1.0
9.5
24.9
16.4
55.7

25.6
35.7
62.4

13.5
18.2

1.2
9.9
22.9
17.5
54.1

27.3
35.0
56.1

13.5
16.3

Day 60

1.1
9.6
23.9
18.2
56.0

13.4
16.1
28.6
34.3
55.7

1.1
9.0
21.2
18.0
56.0

13.3
15.3
23.3
33.6
53.1

1.2
10.0
25.0
18.3
52.0

25.9
36.8
58.5

13.2
16.4

1.3
8.6
22.2
15.5
56.6

25.5
33.0
56.6

12.4
15.3

Day 240

Day 120

Table 7. Changes in DTPA-extractable Pb (pg g-') as affected by sludge application and metal-salt spiking under two ambient temperatures

1.2
10.5
23.1
17.1
52.3

27.8
34.7
56.2

13.1
19.2

1.3
10.3
23.0
15.9
52.4

24.1
32.6
57.9

13.0
15.3

Day 360

"t(

&

B
a

%
0

t,

Bioavailability of Cd and Pb

109

change in Cd extractability over time, and of any effect of temperature o n the extraction, together
with a clear decreasing trend in Pb extractability, suggests that the DTPA soil test is not very suitable
for predicting the trends in metal bioavailability under the conditions of this experiment. However,
it has been known for some time that plants grown in pots tend to accumulate trace metals to a
greater extent than they d o under field conditions. Nevertheless, although the data for metal
accumulation by ryegrass in these experiments may not be directly comparable to field conditions,
the trends indicated are likely to be highly relevant.

CONCLUSIONS
The following conclusions can be drawn from the experiment reported here:

1 . The addition of Cd and P b to soils in either sewage sludge or metal salts resulted in increased
concentrations of these metals in ryegrass, but accumulation was greatest from the metal-spiked

soils.
2. The uptake of metals by ryegrass from all treatments was significantly higher from the pots in
the warm environment (25C) than from those in the cool environment (15OC).
3. In the sewage sludge treated soils, accumulation of both metals by ryegrass in the cool
environment was significantly lower from the soils treated with sewage sludge at the high rate
(I 50 t ha..') than the accumulation from a low sludge rate (50 t ha-'). Although this could possibly
be due in part to dilution through increased dry matter production, it also appears to highlight the
importance of sewage sludge acting as both a source and a highly adsorptive medium for trace
metals.
4. Accumulation of Cd and P b from the sewage sludge treated soils increased during the residual
period and this appeared to coincide with a decrease in pH.
5 . DTPA-extractable Cd and P b concentrations did not reflect the changes in metal uptake by
ryegrass associated with temperature, time and sludge rate.

ACKNOWLEDGEMENT
One of us (PSH) was in receipt of a n Academic Staff Award from The Association of
Commonwealth Universities (UK).

REFERENCES
H. 1990.
ALLOWAY,
B.J., JACKSON,
A.P. & MORGAN,
The accumulation of cadmium by vegetables grown
on soils contaminated from a variety of sources.
Science of The Total Environment 91,223-236.
ALLOWAY,
B.J. & JACKSON,
A.P. 1991. The behaviour
of heavy metals in sludge-amendedsoils. Science of
The Total Environment 100, I51 176.
AvEnY, B.W. & BASCOMB,
C.L. 1974. Soil Survey
Methods, Technical Monograph Number 6. Soil
Survey of England and Wales, Harpenden.
BIDWELL,
A.M. &DOWDY,
R.H. 1987. Cadmium and
zinc availability to corn following termination of
sewage sludge applications. Journal of Environmental Quality 16,438-442.
CHANG,
A.C., PAGE,A.L. & BINGHAM,
F.T. 1982.
Heavy metal absorption by winter wheat following
termination ofcropland sludgeapplication.Journal
v f E n v ~ r ~ n r n e nQuulity
t ~ ~ 1 11,705-708.
CHANG,
A.C., PAGE,
A.L. & WARNEKE,
J.E. 1983. Soil
conditioning effects of municipal sludge compost.
Journal of Environmental Engineering ( N Y ) 109,
574-583.

CHANG,A.C., PAGE,A.L. & WARNEKE,

J.E. 1987.
Long-term sludge application on cadmium and zinc
accumulation in Swiss chard and radish. Journal of
Environmental Quality 16,217-221.
CHAO,T.T. 1972. Selective dissolution of Mn oxides
from soils with acidified hydroxylamine hydrochloride. Soil Science Society of America Proceedings 36,764-768.
COREY,
B.R., KING,L.D., LUE-HING,
C., FANNING,
D.S., STREET,
J.J. & WALKER,
J.M. 1987. Effects of
sludge properties on accumulation of trace elements
by crops. In Land Application of Sludge-Food
Chain Implications (eds A.L. Page, T.J. Logan &
J.A. Ryan), pp. 25-51. Lewis Publishers, Inc.,
Chelsea, MI.
DAY,P.R. 1965. Particle fractionation and particle
size analysis. In Methods qfSoilAnalysis, Part I (ed.
C.A. Black), pp. 545-567. American Society of
Agronomy, Madison, WI.
DEHAAN,
S. 1975. Land application of liquid mnnicipal wastewater sludges. Journal of Water Pollution
Control 47,2707-2710.

110

P.S. Hooda & B. J. Allowuy

EPSTRIN,
E. 1975. Effect of sewage sludge on some soil
physical properties. Journal of Environmental
Quality 4, 139-142.
EKIKSSON,
J.E. 1989. The influence ofpH, soil type and
time o n adsorption and uptake by plants of Cd
added to the soil. Water, Air and Soil Pollution 48,
317- 335.
HECKMAN,
J.R., ANGLE,J.S. & CHANEY,
R.L. 1987.
Residual cffccts of sewage sludge on soybean: I .
Accumulation of heavy metals. Journal uf
Environmentul Qua1it.y 16, 113 1 17.
HI;SSE, P.R. 1971. A Textbook (f Soil Chemical
Anu/,ysis.John Murray, London.
HINESLY,
T.D., ZIEGLEK, E.L. & BARKETT, G.L. 1979.
Residual cffccts of irrigating corn with digested
scwagc sludge. Journal qfEnvirunmenta1 Quality 8,
35 -38.
JACKSON,
A.P. & ALLOWAY,
B.J. 1991. The bioavailability of cadmium to lettuces and CdbbgeS in soils
previously treated with sewage sludges. Plunt and
S(>il132, 179-186.
KEEFEK,R.F., SINGH,R.N. & HORVATH,
D.J. 1986.
Chemical composition of vegetables grown on an
agricultural soil amended with sewage sludge.
.lournu/ ufEnvironmenta1 Quality 15, 1 4 6 ~152.
KOKCAK,R.F. & FANNING,D.S. 1985. Availability
of applied hcavy mctals as a function of type of
soil material and metal source. Soil Scimcc. 140,
23 34.
LINDSAY,
W.L. & NORVEIL,
W.A. 1978. Development
of DTPA test for zinc, iron, manganese, and
copper. Soil Science Society of Amrricu Journul42,
421 428.
MACLEAN,A.J. 1976. Cadmium in different plant
spccics and its availability in soils a s influenced by
organic matter and addition of lime. Canadiun
Jovmul uf Soil Scicvm 56, 129 138.
MAIILEK,
R.J., BINGHAM,
F.T., S ~ o s l r oG.
, & PAGE,
A.L. 1980. Cadmium-cnrichcd scwagc sludge application to acid and calcereous soils: relation between
treatment, cadmium in saturation extracts, and
cadmium uptake. Journal (if Environmental Quulity
9,359 364.

MCGKATH,S.P. 1987. Long-term studies o f metal

transfers following application or sewage sludge. In
Pollutant, Transport and Fute in Ecosystenz.7 (eds
P.J. Coughtrey, M.H. Martin & M.H. Unsworth),
pp. 301- 317. Blackwell Scientific Publications,
Oxrord.
MOKEL,J.L., P I E K K A T , J.C. & GUCKEKT, A. 1988.
Effect of lime and ferric chloride-treated urban
sewage sludge on the concentration of some heavy
metals in corn. Agronnmie8,107 113.
NARWAL,
R.P., SINGH,B.R. & PANHWAK,
A . R . 1983.
Plant availability of heavy metals in sludge-treated
soils: I . Effect of sewage sludge and soil pH on yield
and chemical composition of rape. Journal uf
Environmentul Quulity 12,358 365.
RAPPAPORT,
B.D., MAKTCNS,
D.C., R E N E AJK.,
~ J R.B.
& SIMPSON,
T.W. 1988. Metal availability in sludgeamended soils with elevated metal levels. Journul uf
Environmental Quality 17,42 47.
ROBERTSON,
W.K., LUTRICK,M.C. & YUAN,T.L.
1982. Heavy application of liquid-digested sludge
on three soils: 1. Effects on soil chemistry. JournuIqf
Environmental Quality 11,278-282.
SANDERS,
J.R., MCGKATH, S.P. & ADAMS,T. MCM.
1987. Zinc, copper and nickel concentrations in soil
extracts and crops grown on four soils treated
with metal loaded sewage sludges. ~nvjr~inmenlul
Pollution 44, 193-210.
SCHAUEK,
P.S., WKIGHT,W.R. & PELCHAT,J. 1980.
Sludge-borne heavy metal availability and uptake
by vegetablc crops under field conditions. Journul (if
Environmentul Quulity 9,69-73.
SILVIEKA,
D.J. & SOMMERS,
L.E. 1977. The extractability of copper, zinc, cadmium, and lead in soils
incubated with sewage sludge. Journul of Environm(wu1Quality 6,47-52.
SOON,Y.K. &BATES,T.E. 1985. Molybdcnum,cobalt,
and boron uptake from sludge-amended soils.
Canadian Journal of Soil Science 65,507- 517.
TESSIEK,A.P., CAMPBELL,
G.C. & BISSON,M. 1979.
Sequential extraction procedure for speciation of
particulate trace metals. Anulytical Chemi,stry 51,
844-850.

(Received I 7 .January 1992; accepted 25 August 1992)