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Mobility and Uptake of Zn, Cd, Ni and Pb in Sludge-amended Soils Planted to
Dryland Maize and Irrigated Maize-Oat rotation
Zekarias M. Ogbazghi*1, Eyob H. Tesfamariam*1, John G. Annandale1, and Petrus C. De Jager1
1
University of Pretoria, Department of Plant Production and Soil Science, Private Bag: X20, Hatfield
0028, Pretoria, South Africa, Tel: +27124204724.
*Corresponding author ([email protected], [email protected])
Abbreviations:TMT, total maximum threshold; TIL, total investigative level; MAT, maximum
available threshold; EDTA, Ethylenediaminetetraacetic acid; ERWAT, East Rand Water Care Works;
WRC, Water Research Commission
1
ABSTRACT
Sludge application to agricultural lands is often limited, mainly because of concerns about metal
accumulation in soils and uptake by crops. The objective of the study was to test the hypotheses
that in the short to medium term (5-10 years) the application of good quality sludge according to
crop nitrogen requirements: i) will not lead to significant accumulation of water soluble metal
fractions in soil, ii) mobility and uptake of metals is higher under irrigated than dryland systems,
and iii) metal concentrations in plant tissue could reach phytotoxic levels before the soil reaches
environmental threshold levels. Field plots were arranged in a randomized complete block design
comprising four replications of three treatments (0, 8, and 16 Mg ha-1 yr-1 anaerobically digested
municipal sludge) planted to dryland maize and irrigated maize-oat rotation. Soil and plant
samples were collected following 7 years of treatment application for selected metal analyses. A
large fraction of the Zn, Ni, and Pb in the soil profile was EDTA extractable (46 to 79%).
Saturated paste extractable fractions of Cd and Pb were <1 mg kg-1. Plant uptake of Cd, Pb and
Ni under irrigation was double that for dryland systems. Concentrations of the metals considered
in plant tissue of both cropping systems remained well below phytotoxic levels, except for Zn
under dryland maize that received 16 Mg sludge ha-1 yr-1. Metal concentrations in the soil
remained far below total maximum threshold levels. Therefore, hypotheses 1 and 3 were
accepted for the metals considered and hypothesis 2 was rejected for Zn.
2
Introduction
The use of sewage sludge for crop production is a well-known practice around the world
because of its soil conditioning effect and as a source of low grade fertilizer (Gasco and Lobo,
2007; Herselman, 2010). Sewage sludge, when applied to agricultural soils, can substitute
inorganic fertilizers and improve soil physical properties. However, one of the main concerns for
sustainable use of municipal sewage sludge on agricultural soils, is the long term build-up of
trace metals (Smith, 2009). Some trace metals (e.g., Cu and Zn) are essential for plant and
animal health. However, concentrations exceeding threshold levels have the potential to cause
toxicity to plants and animals (Sterritt and Lester, 1984). Other heavy metals (e.g., Cd and Pb)
are not known to be essential to plants and animals. Toxicity, however, occurs when metals are
concentrated in the environment above threshold levels.
Finding environmentally acceptable, socially responsible, and economically feasible ways
of using municipal sewage sludge has received much attention from both the research
community and regulatory agencies, as well as from the general public. Land application
provides a means of supplying nutrients, such as nitrogen (N) and phosphorus (P), and organic
matter (OM), and can be both agriculturally useful and environmentally responsible. However,
application of sludge has led to concerns on how potential contaminants (heavy metals, organic
contaminants and pathogens) may pollute the groundwater underlying application areas.
Generally the natural background concentration of heavy metals in soils plays a determining role
in the level of threat to groundwater pollution from any anthropogenic additions such as through
the application of sludge. The background concentration of a soil is defined as the normal
chemical composition of an earth material prior to its contamination (Korte, 1999). The
background concentration is a function of the parent material and soil formation processes and is
3
therefore highly variables across regions. For instance, in many South African soils, the natural
background concentrations of Ni, Zn, and Pb is high (Herselman et al., 2005). Therefore,
extreme caution is needed when applying sludge to agricultural soils.
Previous studies have shown that heavy metal uptake by crops increases as sludge
application rate increases (Hinesly et al., 1978; Bidwell and Dowdy, 1987; Kiemnec et al., 1990;
Logan et al., 1997). Heavy metal uptake by crops is influenced by metal concentration in the soil,
as well as soil physical and chemical properties (Merrington, et al., 2003). Other studies reported
an increase in soil metal concentrations as sludge application rate increased in fields where crops
were not planted (Williams et al., 1984). Few studies have investigated the effect of sludge
application on crop heavy metal uptake and accumulation in the soil profile (Soon et al.,1980;
MacLean et al., 1987; Granato et al., 2004; Fuentes et al., 2006). The movement of heavy metals
in sludge amended soils (Emmerich et al., 1982; Yingming and Corey, 1993), mass balance and
distribution of sludge-borne trace elements following long-term application of sewage sludge
(Baveye et al., 1999), and influence of sewage sludge application on soil properties, distribution
and availability of heavy metal fractions (Tsadilas et al., 1995) has also been investigated.
However, to our knowledge, there is no information on the effect of soil water availability
(dryland vs. intensive irrigated cropping systems) on the dynamics of metals in the soil-plant
system (metal crop uptake and partitioning between plant organs, fate and mobility within the
soil system) from class A (U.S. EPA, 1995), or class A1a (South Africa, Snyman and Herselman
(2006)) sludge amended soils under controlled short to medium term field experiments. In
addition, the unwritten rule of using environmental soil contamination threshold values as
phytotoxicity indicators needs to be investigated. Similarly, little is known about the dynamics of
these metals with respect to the relationship between total concentration, plant available and
4
water soluble fractions of metals from sludge amended soils under dryland vs. irrigated systems.
This study focuses on Zn, Cd, Ni and Pb, which are four of the eight elements of concern listed
in the South African agricultural sludge guideline (Snyman and Herselman, 2006). These four
are selected because of their potential reactivity, toxicity, mobility and availability in South
African soils and sludges.
The objective of the study was to test the hypotheses that in the short to medium term (5-10
years) the application of agricultural quality sludge according to crop nitrogen requirements: i)
will not result in a significant increase in the water soluble content of heavy metals in the soil, ii)
mobility and uptake of heavy metals for an irrigated maize-oat rotation will be higher than for
dryland maize, and iii) the concentration of heavy metals in plant tissue could reach phytotoxic
levels before the soil reaches environmental threshold levels.
Materials and Methods
Field Site Description
The study was conducted at the East Rand Water Care Works (ERWAT), Johannesburg,
Gauteng, South Africa (26o 01’ 01” S; 28o 16’ 55” E; altitude 1577 m above sea level). The area
has a long term annual average rainfall of 700 mm, mainly from October to March. The soil of
the experimental site is a clay loam (Hutton; Soil Classification Working Group, 1991) having a
clay content of 36 to 46%, and pH (H2O) of 5.3 to 6.1. In the beginning of the study, the cation
exchange capacity of the soil (ammonium acetate extract) was 12 cmolc kg-1 and the electrical
conductivity of the saturation paste extract ranged from 8 mS m-1 at 1.2 m depth, to 36 mS m-1 in
5
the top 0.3 m soil layer. Initial concentration of Zn, Cd, Ni, Pb and other chemical properties of
the soil for the study site are provided in Table 1.
Table 1 Initial chemical properties and concentration of selected metals in a clay loam Hutton
soil.
Zn
Cd
Ni
Pb
P-
Exchangeable
Bray1
K
N
matter
mg kg-1
10.35
0.018
29.48
14.85
Organic
%
43.9
24.63
0.13
2.98
Field Trials and Treatments
Plots of 25 m2 were arranged in a randomized complete block design comprising four
replications of three sludge application rate treatments. The trial was laid out to accommodate
widely different levels of bio-solid application to high and low productivity-cropping systems. It
consisted of two farming systems namely: dryland maize and an irrigated maize-oat rotation. The
two contrasting cropping systems were selected to represent a dryland (rainfed) farming system
on the one hand and an intensive irrigated system on the other hand. This created a range of
conditions affecting nutrient and metal mobility and uptake. Maize was selected as test crop
because it is one of the most widely cultivated crops across the globe and accounts for 51% of
the cultivated land in South Africa (FAO, 2005). Oats were planted as a rotation crop because of
its dual benefits: healthy grain for human beings (Peterson, 1992) and a high quality fodder for
animals (Schrickel et al., 1992) and can be planted (under irrigation) during winter as rotation
crop in the summer rainfall areas or can be alternated with legume crops in summer.
6
The treatments for dryland maize and irrigated maize-oat rotation consisted of two sludge
rates (8 and 16 Mg ha-1 yr-1), and a zero control. The value of 8 Mg ha-1 yr-1 represents the annual
agricultural upper limit of the 1997 South African sludge guideline (WRC, 1997) which has
recently been raised to 10 Mg ha-1 yr-1 (Snyman and Herselman, 2006). Sludge rates of 16 Mg ha1
yr-1 represent double the former norm. Sludge was applied since the 2004/05 until the 2011/12
summer season. For the irrigated maize-oat rotation, the annual sludge application was split into
two, with half applied to both crops at planting. For dryland maize, however, the entire amount
was applied at the beginning of the season before planting. Sludge was broadcast and
immediately incorporated into the top soil (0.3 m) with a manually operated, diesel powered
rotovator (Agria). After sludge incorporation, the soil was leveled using rakes and maize (CV.
PAN 6966) was planted in 0.9 m rows at rates of 80000 seeds per hectare under irrigation and
half this rate under dryland conditions. Each plot consisted of 6 rows 5 m in length, with the
outer row on either side taken as border rows. After harvesting irrigated maize, sludge was
applied accordingly and again incorporated, after which oats were planted. Oats were planted at a
rate of 90 kg ha-1 using a hand-drawn planter with double disk openers. Each oat plot consisted
of 15 rows, spaced 0.3 m apart and 5 m in length, with two border rows on either side.
Sludge Characteristics
The sludge used in this study was anaerobically digested and paddy-dried. According to the
current South African sludge guideline (Snyman and Herselman, 2006), this sludge is classified
as pollutant class “A” because of its low heavy metal content (Table 2). Based on the
microbiological report from the East Rand Water Care Works (ERWAT) laboratory, the sludge
7
can also be classified as microbiological class “a”. Considering the low odour and vector
attraction characteristics of the sludge, it can also be classified as stability class 1.
Table 2 New three-tier system for the classification of South African sludges (Snyman and
Herselman, 2006).
Pollutant Class (mg kg-1)
A
B
C
Zn
<2800
2800-7500
>7500
Cd
<40
40-85
>85
Ni
<420
420
>420
Pb
<300
300-840
>840
Stability Class
1
Low odour and vector attraction
2
3
Medium attraction
High odour and vector attraction
Microbiological Class
Faecal coliform
a
b
c
<104
106-107
> 107
<1
1-4
>4
(CFU/gdry)
Helminth ova
(Viable ova/gdry)
The current South African sludge guideline (Snyman and Herselman, 2006) allows such
quality sludges to be utilized in agriculture without restriction, as long as the N applied does not
exceed crop demand, with the upper limit set at 10 Mg ha-1 yr-1. Selected chemical characteristics
of this class A1a sludge are presented in Table 3.
8
Table 3 Chemical characteristics of anaerobically digested, paddy dried sludge used during the
2004/05–2010/11 growing seasons (Source: Vlakplaas wastewater treatment plant).
Element
Unit
Year
2004/05
2005/06
2006/07
2007/08
2008/09
2009/10
2010/11
N
g kg-1
30.3
18.8
22.2
30.9
27.4
22.4
27.5
P
g kg-1
19.6
18.4
27.6
22.4
34.3
31.3
42.1
P-Bray1
mg kg-1
166
154
40
66
50
80
120
Total C
g kg-1
230
200
210
200
212
166
219.6
K
mg kg-1
3804
710
689
1356
1720
2530
1850
Ca
mg kg-1
25116
13062
17450
10042
26950
23147
28312
Mg
mg kg-1
25116
13062
17450
10042
26950
23147
29312
pH
H 2O
6.01
6.2
6.02
6.08
8.1
5.7
5.6
Cd
mg kg-1
1.63
0.07
0.15
18.9
19
12.2
10.75
Hg
mg kg-1
1.70
0.02
0.03
1.81
1
1
0.4
Cr
mg kg-1
51.93
1.50
2.92
503.8
419
369.7
315.8
As
mg kg-1
7.08
0.18
0.23
17.94
6.5
5.88
5.64
Pb
mg kg-1
54.46
19.41
61.37
102
75
88.4
66.67
Zn
mg kg-1
459.9
40.3
200.8
2325
4920
3459
5755
Ni
mg kg-1
23.83
10.37
50.97
144.50
152.00
99.30
103.27
Cu
mg kg-1
97.2
3.21
4.59
526.8
681
497.29
544.52
9
Selection of metals
This study focuses on Zn, Cd, Ni and Pb because of their potential reactivity, toxicity,
mobility and high natural background concentration in most South African soils, as well as high
availability in local municipal sludges (Herselman et al., 2005). Cadmium is one of a very small
group of metals which the Food and Agriculture Organization/World Health Organization have
set a provisional daily intake limit for humans (70 µg Cd/day) (Berglund et al., 1983). Cadmium
and lead are considered as the most mobile heavy metals (McLaughlin et al., 2000) and their
concentration in plants is highly correlated with that found in soil (Pais and Benton, 1997).
Irrigation Scheduling
The irrigated maize-oat rotation experiment was planted under drip irrigation. The lateral
spacing between dripper lines was 0.5 m from the summer 2005/06 season, but was reduced to
0.3 m after the 2005 winter season for the rest of the study period. Dripper spacing was 0.3 m in
the laterals. The drip system was operated at a pressure of 100 to 150 kPa with an average drip
rate of 13.8 mm hr-1. In the absence of rainfall, maize was irrigated 10 mm every three days for
the first four weeks after planting. In 2005, this was followed by irrigation according to the FAO
crop factor method in the Soil Water Balance (SWB) model (Jovanovic and Annandale, 1999)
once every five days until harvest in the absence of rainfall. During the growing seasons of 2007
to 2011, however, maize was irrigated according to neutron probe deficit readings to fill the
profile to field capacity once a week in the absence of rainfall. During the winter seasons of each
year, oats were irrigated every three days (9 mm in 2005 and 10 mm in 2006 and 2008) for the
first four weeks. This was followed by irrigations to field capacity according to a site calibrated
10
neutron water meter readings (Model 503 DR CPN Hydroprobe, Campbell Pacific Nuclear,
California, USA) to a depth of 1.2 m for the rest of the season until harvest, mostly twice a week
in 2005 and once a week during the rest of the study period.
Plant and Soil Sampling
In the 2010/11growing season, whole plant (above-ground) samples were collected for
heavy metal uptake determination from an area of 0.5 m2. Two plants per plot were taken under
dryland maize and four under irrigated maize. A hand grab of additional plant samples were
collected randomly from all plots during the 2010/2011 growing season for above-ground
biomass determination.
After harvest, three soil samples were collected diagonally across each plot of a treatment
at 0.3 m depth intervals down to 1.2 m using an auger. The samples were collected from the 0 to
0.3 m, 0.3 to 0.6 m, 0.6 to 0.9 m, and 0.9 to 1.2 m layers. The three samples from each layer of a
plot were combined and mixed to make a single homogenous composite soil sample per layer
(typically 48 soil samples were prepared for each cropping system).
Plant and Soil Chemical Analyses
Plant material was washed using distilled water to remove adhered soil particles and
subsequently pulverized using a stainless steel shredder. All shredded maize plants (including
stems, leaves, cobs and grains) were dried at 80°C for 72 hours and milled using a stainless steel
mill. Plant samples (maize and oat stover, and maize grain) were analyzed for heavy metals after
wet acid digestion using an inductively coupled plasma optical emission spectrometer (ICP11
OES) (SpectroFlame Modula; Spectro, Kleve, Germany), following standard procedures (Nonaffiliated Soil Analyses Work Committee, 1990). Plant toxicity level was assessed based on the
reference values provided by Jones (2012) (Table 4).
Table 4 General phytotoxic and acceptable levels of heavy metals in plant leaf tissue (dry mass)
(Jones, 2012).
Heavy metal
Normal
Toxic
Excessive
mg kg-1
Zn
10 - 100
100 - 150
150 – 400
Cd
0.05 - 0.20
0.20 - 5.0
5 – 30
Ni
0.50 - 10.0
10 - 50
50 – 100
Pb
5 – 30
30 - 100
100 – 300
Corresponding soil samples were air dried, pulverized and sieved using <2 mm sieves prior
to acid digestion and analyzed using aqua regia (75% HCl, 25% HNO3) for total metal
concentration, and Ammonium Ethylenediaminetetraacetic acid (NH4-EDTA) for available
heavy metal concentration. Soil samples were also analyzed for pH (H2O) and Carbon (C) using
a Carlo Erba NA1500 C/N analyzer (Carlo ErbaStrumentazione, Milan, Italy). The threshold
level of selected heavy metals in sludge amended soils was assessed as stipulated in the South
African sludge guideline (Table 5), and guidelines for maximum permissible metal concentration
in agricultural soils from other countries around the globe (Table 6). According to the current
South African sludge guideline (Snyman and Herselman, 2006), the risk to the environment is
unacceptable when the total metal content of the soil exceeds the total maximum threshold
12
(TMT) level. If the total metal content of the soil is between total investigative level (TIL) and
the TMT (Table 5), the mobility of the metals concentration in the soil needs to be assessed.
Table 5 Metal limits for sludge amended soils (Snyman and Herselman, 2006).
Metal
Total Investigative
Total Maximum
elements
Level (TIL)
Threshold (TMT)
(aqua regia)
(aqua regia)
Maximum Available
Threshold
(MAT) (NH4NO3)
mg kg-1
Zn
185
200
5.0
Cd
2
3
0.1
Ni
50
150
1.2
Pb
56
100
3.5
Table 6 Guidelines for maximum permissible metal concentrations in agricultural soil across
regions.
Heavy metal
S.A. Sludge guideline1
Europe2
USA3
Australia &
New Zealand2
mg kg-1
1
Zn
200
150-300
1400
200
Cd
3
1-3
20
3
Ni
150
30-75
210
60
Pb
100
50-300
150
300
Snyman and Herselman (2006)
2
McLaughlin et al. (2000)
13
3
US EPA (1995)
Total investigate level (TIL) is a flag that warrants detailed soil analyses in terms of
mobility using NH4NO3 extraction. If the NH4NO3 extractable metal content of the soil exceeds
the maximum available threshold (MAT), sludges of pollutant class B may not be applied to this
soil. If the NH4NO3 extractable metal content of the soil is lower than the MAT, sludge of
pollutant class B can be applied to the soil and the land should be re-assessed two years after
sludge application (Snyman and Herselman, 2006). The soluble fraction of soil heavy metals was
also analyzed using saturated paste extracts. The saturated pastes were prepared by adding
deionized water to 250 g of air-dried samples until it reached a condition of complete saturation,
as described by the standard procedures in Non-affiliated Soil Analyses Work Committee
(1990). Saturated pastes were allowed to equilibrate for 24 hours in a covered container. An
extract from the saturated paste was acquired by filtering the soil paste through Whatman no 50
paper on a Buchner funnel under low suction (20 kPa).
Statistical Analyses
Statistical analyses were performed to evaluate the effect of varying sludge application
rates on heavy metal uptake by dryland maize, irrigated maize and oat, and concentrations in the
soil. The statistical analyses were conducted using Analysis of Variance (ANOVA) and General
Linear Model (GLM) procedures of Windows SAS Version 9.3 (SAS Institute, 2010) to
determine significant treatment effects on measured response variables. When treatment effects
were found to be significant, Fisher’s protected LSD test at the 0.05 level was used to separate
means.
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Result and Discussion
Heavy Metal Uptake by Crops
Zinc (Zn)
Zinc uptake by both dryland maize and the irrigated maize oat-rotation increased
significantly as sludge application rate increased (Fig. 1a). This is in agreement with previous
findings by Hinesly et al. (1978), who reported a significant increase in Zn uptake by maize (20
inbred lines) as sludge application rate increased. Generally Zn uptake was significantly lower
for the irrigated maize than for dryland maize treatments receiving similar levels of sludge,
except for the 16 Mg ha-1 yr-1 treatment, where uptake by dryland maize was relatively higher,
although not significantly so. Nonetheless, the annual Zn uptake by the irrigated maize-oat
rotation from sludge amended treatments was significantly higher than similar dryland maize
treatments. The lower Zn uptake by the irrigated maize is mainly attributed to the reduction in Zn
plant availability because of the extra Zn removal by oats (Fig. 1b) during the winter season. The
amount of Zn taken up by oats was generally lower than similar irrigated maize treatments (Fig.
1b) despite receiving similar Zn amounts. Such variations in Zn uptake between crops and within
cultivars of a specific crop are common (Hinesly et al., 1978; Alloway, 1995).
It was also apparent that Zn stored in the stover (stems and leaves) was significantly higher
than that in the grain (Fig. 1b). Previous studies conducted by Hinesly et al. (1978) and Granato
et al. (2004) also report similar results. Grain Zn storage accounted for 13 to 19%, 30 to 33%,
and 22 to 27% of the total crop aboveground biomass Zn uptake from the 0, 8 and 16 Mg ha-1 yr1
sludge treatments, respectively, by dryland and irrigated maize-oat rotation. The fraction of Zn
stored in maize grain from the 8 Mg ha-1 yr-1 and 16 Mg ha-1 yr-1 treatments were similar to the
15
low-medium (33 – 36%), and high (26%) sludge application treatments of Bidwell and Dowdy
(1987), respectively. Similarly, the fraction of Zn in maize grain from the 8 Mg ha-1 yr-1 sludge
treatment was closer to the findings of Shivay and Prasad (2014) (34 – 39%) for maize that
received Zn as micro nutrient through foliar and soil applications. The fraction of Zn in maize
grain for the control treatment from this study was much lower than the 63% of Bidwell and
Dowdy (1987), as well as, the 37% of Shivay and Prasad (2014). This is most probably due to
the lower natural background concentration of Zn from this study (0.0155 mg kg-1; total)
compared with that of Bidwell and Dowdy (1987) (9.10 mg kg-1; total) as well as Shivay and
Prasad (2014) (0.36 mg kg-1; plant available).
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Fig.1. Total aboveground biomass zinc uptake by dryland maize, irrigated maize and irrigated
maize-oat rotation (a), and zinc uptake by maize stover vs. grain (b) as well as concentration of
zinc in stover and grain of dryland maize and irrigated maize-oat rotation (c) planted to a clay
loam Hutton soil treated with municipal sludge at varying rates for seven years.
The low grain Zn concentration is an indication of low Zn transfer from vegetative biomass
to the grain (Fig. 1b). Similar to the patterns of total Zn uptake, Zn uptake by stover and grain
increased as the sludge application was doubled under both cropping systems but was only
significant under dryland (Fig. 1b). It was interesting to note that the concentration of Zn in
maize stover (Fig. 1c) under dryland production, reached phytotoxic levels (103 mg kg-1) for the
16 Mg ha-1 yr-1 sludge treatment following the reference values provided by Jones (2012) in
Table 4. This is in contrast to soil Zn concentration (95 mg kg-1 near the soil surface) which was
far below environmental threshold levels (185 mg kg-1) stipulated by South African sludge
guideline (Table 5) as well as other international guidelines for maximum permissible metal
concentration in agricultural soils (Table 6). The high dryland maize Zn concentration under the
16 Mg ha-1 yr-1 application rate, is most probably attributed to a combination of factors, including
relatively low biomass production (Tesfamariam, 2009) and therefore lower crop Zn uptake over
the 7 consecutive years of this study compared with the irrigated system, which might have
resulted in the buildup of Zn in the soil. This is in agreement with previous findings who
reported high Zn uptake at high sludge application rates because of Zn accumulation in the soil
(Miller et al., 1995; Kalbitz and Wennrich, 1998; and Merrington et al., 2003). The high Zn
uptake observed at high sludge application rates under dryland maize relative to equivalent
irrigated maize-oat rotation is mainly attributed to the increase in the amount of Zn added to the
soil with the sludge. The observed reduction in soil pH as the sludge application rate increased
17
(Table 7) could have also contributed to such increase in Zn uptake. This is in agreement with
previous findings of Miller et al. (1995), who reported that, Zn uptake is mainly associated with
high metal concentrations in sludges, and/or low soil pH values of 4.5 – 6.
Table 7 Soil pH (H2O) and organic C (%) in the soil profile of both dryland maize and irrigated
maize-oat rotation for the growing season of 2010/11.
Soil pH (H2O)
Soil C (%)
Sludge application rates
Sludge application rates
Mg ha-1
Cropping system
Dryland maize
Irrigated maize-oat rotation
Soil depth (m)
0
8
16
0
8
16
0 – 0.3
6.54
5.68
5.44
1.37
1.52
1.58
0.3 – 0.6
6.27
5.76
6.07
0.8
0.94
0.81
0.6 – 0.9
5.89
5.90
5.81
0.39
0.48
0.53
0.9 – 1.2
5.81
5.78
5.44
0.28
0.39
0.31
0 – 0.3
7.1
6.83
6.00
1.4
1.54
1.64
0.3 – 0.6
6.47
6.72
6.60
0.92
0.94
0.77
0.6 – 0.9
6.4
6.44
6.53
0.46
0.58
0.43
0.9 – 1.2
6.07
6.03
6.16
0.33
0.42
0.27
The increasing trend in Zn uptake observed in this study strengthens concerns raised by
Lotter and Pitman (1997), who point out that uncontrolled utilization of sewage sludge on
agricultural lands will lead to accumulation of Zn in the receiving soil, which could lead to a
permanent risk to plants, and thereby compromise sustainability.
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Cadmium (Cd)
Cadmium uptake by dryland maize and irrigated maize-oats also increased significantly as
sludge application rate increased (Fig. 2a). Generally, Cd uptake by irrigated maize was higher
than for dryland maize treatments (Fig. 2a). This is in contrast to Zn uptake, which was relatively
lower for equivalent irrigated maize treatments. This indicates that the mobility of Cd from soil
to crop is influenced by the availability of soil water. This leads to the acceptance of hypothesis 2
“Uptake of heavy metals under irrigated maize-oat rotation is higher than dryland maize” for Cd.
This supports previous findings that the mobility of Cd in the soil-plant system is greater than for
Zn (Sauerbeck, 1991; McLaughlin et al., 2000; Legind et al., 2012). Similar to Zn, the amount of
Cd stored in stover was significantly higher than the grain under both cropping systems (Fig. 2b).
It was also interesting to note that Cd uptake by stover and grain significantly increased as the
sludge application rate increased. This is attributed to the increase in Cd concentration in the soil
at higher sludge levels and is highly correlated to plant uptake (Pais and Benton, 1997).
Cadmium in the grain of both cropping systems accounted for 38 to 45% of the total
aboveground biomass Cd uptake, indicating the mobility of Cd within the plant system. This is in
contrast to the 13 to 33% for Zinc. The fraction of Cd in maize grain relative to the total
aboveground biomass Cd uptake from this study was higher than the 3-12% of Bidwell and
Dowdy (1987). Such big differences could most probably be because of the genetic differences
between the cultivars (Hinesly et al., 1978; Alloway, 1995) among other environmental factors.
19
Fig.2. Total aboveground biomass cadmium uptake by dryland maize, irrigated maize and
irrigated maize-oat rotation (a), and cadmium uptake by maize stover vs. grain (b) as well as
concentration of cadmium in stover and grain of dryland maize and irrigated maize-oat rotation
(c) planted to a clay loam Hutton soil treated with municipal sludge at varying rates for seven
years.
The observed increase in Cd uptake by crops as the sludge application rate increased is
mainly attributed to increase in the amount of Cd added to soil. The reduction in soil pH at
higher sludge application rate (Table 7) could have also contributed to the increase in Cd uptake.
This is because the bioavailability of Cd and metals in general increases as the soil pH decreases
20
below 7 (Kalbitz and Wennrich, 1998). Despite the highly mobile nature of Cd, the concentration
within the plant tissue remained below phytotoxic levels (>0.2 mg kg-1) (Fig. 2c) following
seven years of continuous sludge application at varying rates.
Nickel (Ni)
Nickel uptake by both cropping systems increased significantly as the sludge application
rate increased (Fig. 3a). This is mainly attributed to the increase in the amount of Ni added to the
soil. The reduction in soil pH as the sludge application rate increased (Table 7) could have also
contributed to such increase in Ni uptake because bioavailability of metals increases as soil pH
decreases (Kalbitz and Wennrich, 1998). Nickel uptake by irrigated maize was significantly
higher than for dryland maize treatments (Fig. 3a). This is despite the application of only half of
the annual sludge application at planting of the irrigated maize, in contrast to the full application
for the equivalent dryland maize treatments. Annual Ni uptake of 16 Mg ha-1 yr-1 under irrigated
maize-oat rotation was double that of similar dryland maize treatments. This indicates that Ni is
quite soluble and its uptake by maize is influenced by the availability of water. Therefore,
hypothesis 2 “Uptake of heavy metals under irrigated maize-oat rotation is higher than dryland
maize” was accepted for Ni.
21
Fig.3. Total crop nickel uptake by dryland maize, irrigated maize and irrigated maize-oat rotation
(a), and nickel uptake by maize stover vs. grain (b) as well as concentration of nickel in stover
and grain of dryland maize and irrigated maize-oat rotation (c) planted to a clay loam Hutton soil
treated with municipal sludge at varying rates for seven years.
Similar to Zn and Cd, the amount of Ni stored in stover was significantly higher than that
in the grain under both cropping systems (Fig. 3b). Nickel uptake by stover and grain increased
significantly as the sludge application rate increased, except for stover under the 8 Mg ha-1 yr-1
dryland maize, which was not significantly different compared with the zero control. The
22
concentrations in the plant tissue, however, remained below phytotoxic levels (>10 mg kg-1)
(Fig. 3c). Nickel concentration in the grain accounted for 14 to 22% of uptake at lower sludge
application rates of 0 and 8 Mg ha-1 yr-1, and 9 to 14% at 16 Mg sludge ha-1 yr-1. This indicates
that Ni has relatively lower mobility within the plant system than Zn and Cd.
Lead (Pb)
Crop uptake of Pb increased significantly as sludge application rate increased (Fig. 4a).
Similar to Zn, Cd and Ni, this is mainly attributed to the increase in the amount of Pb added to
the soil with the sludge. The reduction in soil pH as the sludge application rate increased (Table
7) could have also contributed to such increase in Pb uptake because heavy metal availability
increases as soil pH drops below 7 (Kalbitz and Wennrich, 1998). It was interesting to note that
the annual aboveground biomass Pb uptake by irrigated maize was significantly higher than for
dryland maize treatments receiving the same amount of sludge. This is despite the application of
only half the annual sludge application at planting of the irrigated maize, in contrast to the full
application for dryland maize. The annual crop Pb uptake by the irrigated maize-oat rotation was
more than double that of dryland maize. Similar to Ni, the uptake of Pb by maize was influenced
by the availability of water. Thus hypothesis 2 was also accepted for Pb. Generally, Pb uptake by
stover was significantly higher than grain uptake, both for dryland maize and the irrigated maizeoat rotation (Fig. 4b). Similarly, both stover and grain Pb uptake increased significantly as the
sludge application rate increased for both cropping systems.
23
Fig.4. Total crop lead uptake by dryland maize, irrigated maize and irrigated maize-oat rotation
(a), and lead uptake by maize stover vs. grain (b) as well as concentration of lead in stover and
grain of dryland maize and irrigated maize-oat rotation (c) planted to a clay loam Hutton soil
treated with municipal sludge at varying rates for seven years.
The amount of Pb in the grain accounted for 20 to 29% of the total Pb stored in the
aboveground biomass for the treatments that received sludge rates of 8 and 16 Mg ha-1 yr-1. This
indicates that Pb has relatively moderate mobility within the plant system. The parallel increase
in Pb uptake as the sludge application rate increased is a good indication of the potential
24
accumulation that could lead to phytotoxicity. Nonetheless, the concentration of Pb in plant
tissues following 7 years of municipal sludge application was far below phytotoxic levels (>30
mg kg-1) (Fig. 4c).
Heavy Metal Accumulation and Mobility in the Root Zone
Zinc (Zn)
The mean soil profile Zn concentration under dryland maize increased significantly as
sludge application rate increased (Fig. 5a). Under irrigated maize-oat, however, the mean soil
profile concentration of the 16 Mg ha-1 yr-1 was lower than that of 8 Mg ha-1 yr-1. This is most
probably because of a higher biomass production from the 16 Mg ha-1 yr-1 (20% higher) than for
the 8 Mg ha-1 yr-1 treatment (Tesfamariam, 2009) during the past six years, which might have
resulted in higher plant uptake. Generally there was no clear pattern of Zn translocation
(leaching) to deeper layers as a function of sludge application rate, but the general pattern
seemed to follow a sinusoidal curve, except for the irrigated 16 Mg ha-1 yr-1 treatment, which had
a sigmoidal pattern with high concentrations in the top 0.3 m layer (Fig. 5b). Nonetheless, there
is a clear indication of Zn translocation to lower layers, which increased as sludge application
rate increased, except for the irrigated 16 Mg ha-1 yr-1 treatment. This is in agreement with
previous findings of Hinesly et al. (1978); Boswell (1975); and Sidle and Kardos (1977), who all
report the movement of Zn below the depth of incorporation in agricultural lands. In contrast,
Ippolito and Barbarick (2008) did not find Zn mobility below 20 cm under dryland wheat
production on a plat-ner loam soil, which received sludge at rates of 0, 6.7, 13.4, 26.8 and 40.3
dry Mg ha-1 every 2 years from 1982 to 2002. The absence of Zn mobility below 20 cm in the
25
Ippolito and Barbarick (2008) study, is most probably attributed to the low rainfall of the study
site (350 mm) compared with our study site, which has a long-term annual rainfall of 700 mm. It
was apparent that Zn distribution in the soil profile (Fig. 5a) seems to have similar patterns to
that of soil organic matter (Table 7), which agrees with the findings of Antoniadis and Alloway
(2002), who report a direct relationship between organic matter and Zn concentration in sludge
amended soils.
The overall concentration of Zn in the soil profile of all treatments was still far below the
total investigative level (185 mg kg-1) of the South African sludge guideline (Table 5) and
international guidelines for maximum permissible metal concentration in agricultural soils (Table
6). However, the increase in Zn concentration by 250% following 7 years of 16 Mg ha-1 yr-1
sludge applications indicate the potential for future build up. A large fraction of the total Zn for
both dryland maize and irrigated maize-oat rotation was EDTA extractable or plant available.
The water soluble fraction was, however, well below 1% of the total concentration throughout
the profile, indicating that water soluble Zn was not the main contributor to the translocation of
heavy metals. Therefore hypothesis 1, “Continuous use of good quality sludge with low heavy
metal content will not result in a significant accumulation of water soluble heavy metal fraction
in the short term” was accepted.
Cadmium (Cd)
The mean Cd concentration in the soil profile of both dryland maize and the irrigated
maize-oat rotation system, increased significantly as the sludge application rate increased (Fig.
5c). Similar findings were reported by Baveye et al. (1999) on a liquid sludge treated silt loam
26
soil, where the total concentration of Cd increased as sludge application rate increased. There
was, however, no significant difference between dryland maize and irrigated maize-oats that
received the same sludge application rates. It was also interesting to note that most of the Cd for
the 16 Mg ha-1 yr-1 dryland maize and irrigated maize-oat rotation accumulated in the top 60 cm
layer and decreased with depth (Fig. 5d). This agrees with findings of Baveye et al. (1999), who
report Cd mobility to a depth of 75 cm, which also decreased with depth. In contrast, relatively
high concentrations of Cd accumulated down to 1 m for the 8 Mg ha-1 yr-1 of both cropping
systems. The distribution of Cd in the top 0.3 m layer and 0.9-1.2 m soil layer (Fig. 5d) followed
similar patterns to soil organic C and pH (H2O) of the corresponding layers (Table 7). This too is
in agreement with the findings of Antoniadis and Alloway (2002), who report an increase in the
mobility and plant availability of Cd at high sludge application rates because of the increase in
dissolved organic matter.
The concentration of Cd in the whole profile of both cropping systems, however, was far
below the total investigative level (2 mg kg-1) of the South African sludge guideline (Table 5),
guidelines from other regions of the world (1-20 mg kg-1) (Table 6), and the global soil mean Cd
concentration of 0.6-1.1 mg kg-1 (Kabata-Pendias and Pendias, 2000). The EDTA extractable and
saturated paste extractable (mobile) Cd fraction in the soil profile of both cropping systems was
below the method detection limit (<1 mg kg-1). This is in contrast to the findings of Baveye et al.
(1999), who reported an increase in the DTPA extractable Cd in the top 45 cm soil layer. This
indicates that the excess accumulated Cd was complexed either with soil minerals or organic
matter within the soil. Therefore, hypothesis 1 was accepted for both cropping systems.
27
Fig.5.
Mean
soil
profile
total
(Aqua
Regia
extractable)
and
plant
available
(Ethylenediaminietetraacetic acid extractable) concentrations of zinc (a), and cadmium (c) as
well as mean soil profile total (Aqua Regia extractable) concentrations of zinc (b) and cadmium
(d), distribution in the top 1.2 m layer of a clay loam Hutton soil treated with class A1a sludge
for seven years (Plant available (Ethylenediaminietetraacetic acid extractable) fraction of
Cadmium was below the method detection limit <1 mg kg-1).
Nickel (Ni)
Nickel accumulation in the soil profile did not increase with doubling of the 8 Mg ha -1 yr-1
norm, both under dryland maize and in the irrigated maize-oat rotation (Fig. 6a). This is in
28
contrast with the patterns observed for Zn and Cd. It was also interesting to note that the mean
soil profile Ni concentration of dryland maize was significantly higher than the same irrigated
treatments. This is most probably because of higher plant uptake (Fig. 3a) and potential leaching
below 1.2 m under irrigation because Ni in sewage sludge is mainly in soluble form and is
readily available for plant uptake as well as leaching (Kabata-Pendias and Pendias, 2000). The
concentration of Ni in the whole profile of both cropping systems, however, is far below the total
investigative level (50 mg kg-1) of the South African sludge guideline (Table 5) as well as other
international guidelines (Table 6).
The increasing Ni concentration towards the bottom of the soil profile (Fig. 6b), under the
irrigated 8 and 16 Mg ha-1 yr-1 treatments provides evidence for possible leaching below the
point of measurement (1.2 m) because of the mobile nature of Ni as reported by Snyman and
Van Der Waals (2004). According to Snyman and Van Der Waals (2004) heavy metals such as
Ni leached 8 cm below the plough layer in a short time and suggest that there is a risk of these
metals moving below the incorporation zone. Unlike Zn and Cd, water-soluble Ni was detected
at low concentration levels (≤1% of the EDTA extractable fraction). Therefore, hypothesis 1 was
accepted for Ni. In addition, considering the low soil profile Ni concentration and the increase in
Ni concentration with depth under irrigated conditions, hypothesis 2 was also accepted for Ni.
Lead (Pb)
Generally the mean Pb concentration in the soil profile of dryland maize was significantly
higher than under irrigation, except for the 16 Mg ha-1 yr-1 sludge treatment (Fig. 6c). Under
irrigated system soil profile Pb concentration increased significantly as sludge application rate
29
increased, which was not the case for the dryland system. A large fraction of the Pb in the soil
profile (46 to 79%) was plant-available (EDTA extractable), but the water-soluble fraction was
below the method detection limit (<1 mg kg-1). Consequently, hypothesis 1 was accepted for
both dryland and irrigated maize-oat rotation.
Lead concentration in the soil profile of the zero control treatment remained the lowest
throughout the profile (Fig. 6d), while the irrigated as well as dryland maize production systems
that received 16 Mg ha-1 yr-1 sludge annually showed an increase in Pb concentration below 0.6
m. This indicates the potential leaching losses that might have occurred during the study period
and could probably be the reason for the reported insignificant difference in soil profile
concentration between the 8 and 16 Mg ha-1 yr-1 treatments under dryland maize production. The
distribution of Pb in the top 0.3 m of the soil profile and between 0.6-0.9 m (Fig. 6d) followed
similar patterns to soil organic C (Table 7). Previous studies conducted by Baveye et al. (1999)
also report significant mobility of Pb in their case, to a depth of 45 cm. The overall concentration
of Pb is, however, below the total investigative level (56 mg kg-1) as stipulated in the South
African sludge guideline (Table 5) as well as those from other countries (Table 6).
30
Fig.6.
Mean
soil
profile
total
(Aqua
Regia
extractable)
and
plant
available
(Ethylenediaminietetraacetic acid extractable) concentrations of nickel (a), and lead (c) as well
as mean soil profile total (Aqua Regia extractable) nickel (b) and lead (d) distribution in the top
1.2 m soil profile of a clay loam Hutton soil treated with class A1a sludge for seven years.
The mean soil profile Pb concentration of the 16 Mg ha-1 yr-1 sludge treatments for dryland
maize and irrigated maize-oat rotation increased by 30.56 and 32.06 mg kg-1, respectively after 7
consecutive years of sludge application. Assuming negligible leaching and constant sludge heavy
31
metal content, annual sludge application rate of 16 Mg ha-1 yr-1 could raise soil Zn concentration
of the study site to total maximum threshold levels after 20, 30 and 145 years, according to the
South African (Snyman and Herselman, 2006), European (McLaughlin et al., 2000), and USA
(US EPA, 1995) guidelines, respectively. Similar application rates would raise soil Cd
concentration to TMT levels after 86 years according to South African and European guidelines,
and 580 years according to USA guideline. Nickel could reach to TMT levels after 370, 140 and
550 years, and Pb after 330, 1100 and 525 years according to the South African, European, and
USA guidelines, respectively. Nevertheless, the potential for leaching observed from this study
warrants monitoring protocols that take into account pollutant distribution within a soil profile
over time.
Heavy Metal Mass Balance (Supply less Uptake Mass Balance)
Heavy metal mass balance based on sludge input less crop output is not the full story
because there are other sources and sinks for these metals, in particular losses through leaching.
Mass balance was calculated by subtracting the metal exported (crop uptake) from the total
applied in sludge.
According to a supply less uptake mass balance of a single year (2010/11), Zn uptake by
crops accounted for only 3 to 5% of what was added with sludge (Table 8). This indicates that
more than 95% of Zn added with sludge should accumulate in the soil profile. This is in
agreement with findings of Chang et al. (1984), who report a significant accumulation of Zn in
the soil profile of sludge amended soils. The negative mass balance of the zero control treatment
indicates that the crop used Zn from the soil reserve. Similar to Zn, based on the mass balance of
Cd applied with sludge less that removed by crop, only 3 to 6% of what was added with the
32
sludge was taken up by the crop under both cropping systems (Table 8). This was the reason for
the significant buildup of Cd observed in the soil profile as the sludge application rate was
doubled (Fig. 5c).
Table 8 Mass balances of Zn, Cd, Ni and Pb under dryland maize and irrigated maize-oat
rotation for the growing season of 2010/11.
Heavy metal
Sludge
Metal Supply
application
Metal Uptake
Dryland
Irrigated
Metal Supply less Uptake
Dryland
Irrigated
Rate
Mg ha-1
Zn
Cd
Ni
Pb
kg ha-1
0
0
0.8482
0.4101
-0.8482
-0.4101
8
46.04
1.1969
0.9049
44.843
45.135
16
92.08
1.4861
1.4012
90.593
90.678
0
0
0.0005
0.0012
-0.0005
-0.0012
8
0.086
0.0016
0.0017
0.0844
0.0843
16
0.172
0.0018
0.0029
0.1702
0.1691
0
0
0.0279
0.0200
-0.0279
-0.0200
8
0.826
0.0395
0.0370
0.7865
0.789
16
1.652
0.0788
0.0970
1.5732
1.555
0
0
0.0085
0.0101
-0.0085
-0.0101
8
0.533
0.0128
0.0141
0.5202
0.5189
16
1.067
0.0158
0.0226
1.0512
1.0444
33
Based on the mass balance of Ni added with sludge less uptake (removed) by crop, there
was a net positive Ni accumulation in the profile of both dryland maize and irrigated maize-oat
rotation (Table 8). Of the total Ni added within a year, only 4.5 to 5.5% of the Ni was recovered
by the plant. The rest either accumulated in the soil profile or leached below the depth of
measurement. Similar to Zn and Cd, the net positive Ni mass balance highlights future potential
accumulation in the soil profile and warrants setting monitoring protocols.
Based on the mass balance of Pb added with sludge less uptake by dryland maize and
irrigated maize-oats, sludge application resulted in a net positive mass balance indicating a
potential build up of Pb in the soil though at a low rate (Table 8). According to this study, only 2
to 5% of the total Pb added to the soil was taken up by the plant with, the rest mostly
accumulating in the soil profile. This provides evidence for possible accumulation or binding of
Pb in sludge-amended soils as reported by Planquart et al. (1999). According to Planquart et al.
(1999) most of the Pb in sludge amended soil was found as an organic matter bound fraction.
Therefore, it is of utmost importance to have integrated management and monitoring
protocols for beneficial agricultural use of sludge in order to minimize potential long-term risks
to human health and the environment in general.
Conclusion
Crop uptake and accumulation in the soil profile of Zn, Cd, Ni and Pb increased as the
sludge application rate increased. Concentrations in tissues of the test crop remained well below
phytotoxic levels, except for Zn under dryland maize production that received sludge at 16 Mg
34
ha-1 yr-1. Concentrations of the selected pollutants in the soil profile of all sludge treatments
remained below threshold levels as stipulated in the South African sludge guideline as well as
international guidelines. A large fraction of these metals was EDTA extractable. The saturated
paste extractable fractions of Cd and Pb were <1 mg kg-1. However, water soluble fractions of Zn
and Ni were detected though <1% of the EDTA extractable fraction, indicating the mobile nature
of these elements and potential for leaching and groundwater contamination. Consequently,
hypotheses 1 and 3 were accepted for the metals studied and hypothesis 2 was rejected for Zn.
Therefore, it is of utmost importance to have integrated sludge management practices and
rigorous heavy metal monitoring protocols below the top 0.3 m plough layer for sustainable
beneficial agricultural use of sludge. Further investigation on metal leaching below the active
root zone is recommended.
References
Antoniadis, V., and B.J. Alloway. 2002. The role of dissolved organic carbon in the mobility of
Cd, Ni and Zn in sewage sludge amended soils. Environ pollut. 117:515-521.
Alloway, B.J. 1995. Heavy Metals in Soils. Blackie Academic and Professional, Glasgow, pp.
368.
Baveye, P., M.B. McBride, D. Bouldin, T.D. Hinesly, M.S.A. Dahdoh, and M.F. Abdel-sabour.
1999. Mass balance and distribution of sludge-borne trace elements in a silt loam soil
following long-term applications of sewage sludge. Sci. Total. Environ. 227:13-28.
35
Berglund, S., R.D. Davis, and P. L. Hermite. 1983. Utilisation of Sewage Sludge on Land:Rates
of application and long-term effects of metals. D. Reidel Publishing Company,
Dordrecht, The Netherlands.
Bidwell, A.M., and R.H. Dowdy. 1987. Cadmium and zinc availability to corn following
termination of sewage sludge applications. J. Environ. Qual. 16:438-442.
Boswell, F.C. 1975. Municipal sewage sludge and selected element application to soil: effect on
soil and fescue. J. Environ. Qual. 4:267-273.
Chang, A.C., J.E. Warneke, A.L., Page, and L.J. Lund. 1984. Accumulation of heavy metals in
sewage sludge-treated soils. J. Environ. Qual. 13:87-91.
Emmerich, W.E., L.J. Lund, A.L. Page, and A.C. Chang. 1982. Movement of heavy metals in
sewage sludge-treated soils. J. Environ. Qual. 11:174-178.
FAO, 2005. Fertilizer use by crops in South Africa. FAO, Rome, Italy.
Fuentes, A., M. Lloréns, J. Saéz, Ma I. Aguilar, A.B. Pérez-Marín, J.F. Ortuňo, and V.F.
Meseguer. 2006. Ecotoxicity, phytotoxicity and extractability of heavy metals from
different stabilized sewage sludges. Environ. Pollut. 143:355-360.
Gasco, G., and M.C. Lobo. 2007. Composition of a Spanish sewage sludge and effects on treated
soil and olive trees. J. Waste Manage. 27:1494-1500.
Granato, T.C., R.I. Pietz, G.J. Knafl, C.R. Carlson, Jr. P. Tata, and C. Lue-Hing. 2004. Trace
element concentrations in soil, corn leaves, and grain after cessation of biosolids
applications. J. Environ. Qual. 33:2078-2089.
Herselman, J.E. 2010. The concentration of selected trace metals in South African soils. Ph.D.
diss., Univ. of Stellenbosch, South Africa.
36
Herselman, J.E., P.W. Wade, C.E. Steyn, and H.G. Snyman. 2005. An evaluation of dedicated
land disposal practices for sewage sludge. WRC Rep. TT 1209/1. Water Research
Commission, South Africa.
Hinesly, T.D., D.E. Alexander, E.L. Ziegler, and G.L. Barrett. 1978. Zinc and Cd accumulation
by corn inbreds grown in sludge amended soil. Agron. J. 70:425-428.
Ippolito, J.A., and K.A. Barbarick. 2008. Fate of biosolids trace metals in a dryland wheat agroecosystem. J. Environ. Qual. 37:2135-2144.
Jones, J.B. 2012. Plant nutrition and soil fertility manual: How to make soil fertility plant
nutrition principles work. 2nd ed. CRC Press. Boca Raton, FL.
Jovanovic, N.Z., and J.G. Annandale. 1999. An FAO crop factor modification to SWB makes
inclusion of crops with limited data possible: examples for vegetable crops. Water SA
25:180-190.
Kabata-Pendias, A., and H. Pendias. 2000. Trace Elements in Soils and Plants. CRC Press, Boca
Raton, Florida.
Kalbitz, K., and R. Wennrich. 1998. Mobilization of heavy metals and arsenic in polluted
wetland soils and its dependence on dissolved organic matter. J. Sci. Total Environ.
209:27-39.
Kickens, L., A. Cottenie, and G. van Landschoot. 1994. Chemical activity and biological effects
of sludge-borne heavy metals and inorganic metal salts added to soils. Plant and soil
79:89-99.
37
Kiemnec, G.L., D.D. Hemphill, Jr. M. Hickey, T.L. Jackson, and V.V. Volk. 1990. Sweet corn
yield and tissue metal concentration after seven years of sewage sludge applications. J.
Prod. Agric. 3:232-237.
Korte, N. 1999. A guide for the technical evaluation of environmental data. Lancaster,
USA:Technomic Publishing Co.
Legind, C.N., A. Rein, J. Serre, V. Brochier, C.S. Haudin, P. Cambier, S. Houot, and S. Trapp.
2012. Simultaneous simulations of uptake in plants and leaching to groundwater of Cd
and Pb for arable land amended with compost or farm yard manure. J. Plos One 7:1-13.
Logan, T.J., B.J. Lindsay, L.E. Goins, and J.A. Ryan. 1997. Field assessment of sludge metal
bioavailability to crops: sludge rate response. J. Environ. Qual. 26:534-550.
Lotter, L.H., and A.R. Pitman. 1997. Aspects of sewage sludge handling and disposal. WRC
Rep. TT 316/1. Water Research Commission, South Africa.
MacLean, K.S., A.R. Robinson, and H.H. MacConell. 1987. The effect of sewage sludge on the
heavy metal content of soils and plant tissue. Commun. Soil Sci. Plant Anal. 18:13031316.
McLaughlin, M.J., B.A. Zarcinas, D.P. Stevens, and N. Cook. 2000. Soil testing for heavy
metals. Commun. Soil Sci. Plant Anal. 31:1661-1700.
Merrington, G., I. Oliver, R.J. Smernik, and M.J. McLaughlin. 2003. The influence of sewage
sludge properties on sludge-borne metal availability. J. Adv. Environ. Res. 8:21-36.
Miller, R.W., A.S. Azzari, and D.T. Gardiner. 1995. Heavy metals in crops as affected by soil
types and sewage sludge rates. Commun. Soil Sci. Plant Anal. 26:737-742.
38
Moreno, J.L., C. Garcia, T. Hernandez, and J.A. Pascual. 1996. Transference of heavy metals
from a calcareous soil amended with sewage sludge compost to barley plants.
Bioresource Technology 55:251-258.
Non-affiliated Soil Analyses Work Committee. 1990. Handbook of standard soil testing methods
for advisory purposes. Soil Science Society of South Africa. Erasmusland, South Africa.
Pais, I., and J. Benton. 1997. The Handbook of Trace Elements. St. Lucie Press, Boca Raton, FL.
Peterson, D.M. 1992. Composition and nutritional characteristics of oat grain and products. In:
H.G. Marshall and M.E. Sorrells, editors, Oat science and technology. ASA, CSSA,
Madison, WI. p. 265-292.
Planquart, P., G. Bonin, A. Prone, and C. Massiani. 1999. Distribution, movement and plant
availability of trace metals in soils amended with sewage sludge composts: application to
low metal loading. J. Sci. Total Environ. 241:161-179.
SAS Institute. 2010. Statistical Analysis Software. Version 9.4. SAS Inst., Cary, NC.
Sauerbeck, D.R. 1991. Plant element and soil properties governing uptake and availability of
heavy metals derived from sewage sludge. Water Air Soil Poll. 57:227-237.
Schrickel, D.J., V.D. Burrows, and J.A. Ingemansen. 1992. Harvesting, storing and feeding of
oat. In: H.G. Marshall and M.E. Sorrells, editors, Oat science and technology. ASA,
CSSA, Madison, WI. p. 751-775.
Shivay, Y.S., and R. Prasad. 2014. Effect of source and methods of Zinc application on corn
productivity, nitrogen and zinc concentration and uptake by high quality protein corn
(Zea mays). Egypt J. Biol. 16:72-78.
39
Sidle, R.C., and L.T. Kardos. 1977. Transport of heavy metals in a sludge-treated forested area.
J. Environ. Qual. 6:431-437.
Smith, S.R. 2009. A critical review of the bioavailability and impacts of heavy metals in
municipal solid waste composts compared to sewage sludge. J. Environ. Int. 35:142-156.
Snyman, H.G., and J. Van Der Waals. 2004. Laboratory and field scale evaluation of agricultural
use of sewage sludge. WRC Rep. TT 1210/04. Water Research Commission, South
Africa.
Snyman, H.G., and J.E. Herselman. 2006. Guidelines for the utilisation and Disposal of waste
water sludge, Volume 2:Requirements for the agricultural use of wastewater sludge.
WRC Rep. TT 262/06. Water Research Commission, South Africa.
Soil classification working group. 1991. Soil classification:A taxonomic system for South Africa.
Dep. of Agric. Development, Pretoria, South Africa.
Soon, Y.K., T.E. Bates, and J.R. Moyer. 1980. Land application of chemically treated sewage
sludge: III. Effects on soil and plant heavy metal content. J. Environ. Qual. 9:497-504.
Sterritt, R.M. and J.N. Lester. 1984. Significance and behaviour of heavy metals in waste water
treatment processes. III. Speciation in waste waters and related complex matrices. Sci.
Total Environ. 34:117–141.
Tesfamariam, E.H. 2009. Sustainable use of sewage sludge as a source of nitrogen and
phosphorous in cropping systems. Ph.D. diss., Univ. of Pretoria, South Africa.
40
Tsadilas, D.C., T. Matsi, N. Barbayiannis, and D. Dimoyiannis. 1995. Influence of sewage
sludge application on soil properties and on the distribution and availability of heavy
metal fractions. Commun. Soil Sci. Plant Anal. 26:2603-2619.
U.S. EPA. 1995. A plain English Guide to the EPA Part 503 biosolids rule. USEPA Rep. 93/003832. U.S. Gov. Print. Office, Washington, D.C.
WRC. 1997. Permissible Utilisation and Disposal of sewage sludge. 1st ed. Water Research
Commission, South Africa.
Williams, D.E., J. Vlamis, A.H. Pukite, and J.E. Corey. 1984. Metal movement in sludge treated
soils after six years of sludge addition: I. Cd, Cu, Pb, and Zn. Soil Sci. 137:351–359.
Yingming, L., and R.B. Corey. 1993. Redistribution of sludge-born cadmium, copper, and zinc
in a cultivated plot. J. Environ. Qual. 22:1-8.
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