Bioresource Technology 70 (1999) 23±31
Heavy metal contents of livestock feeds and animal manures in
England and Wales
F.A. Nicholsona,*, B.J. Chambersa, J.R. Williamsb, R.J. Unwinc
a
c
ADAS Gleadthorpe Research Centre, Meden Vale, Mans®eld, Nottinghamshire, NG20 9PF, UK
b
ADAS Boxworth, Boxworth, Cambridge, CB3 8NN, UK
Farming and Rural Conservation Agency, Nobel House, 17 Smith Square, London SW1 3JR, UK
Received 1 December 1998; revised 18 January 1999; accepted 4 February 1999
Abstract
In this study, 183 livestock feeds and 85 animal manure samples were collected from commercial farms in England and Wales
and analysed to determine their heavy metal (zinc, copper, nickel, lead, cadmium, arsenic, chromium and mercury) contents.
Zinc and copper concentrations ranged from 150±2920 mg Zn/kg dm (dry matter) and 18±217 mg Cu/kg dm in pig feeds,
depending on the age of the pigs. In poultry feeds, concentrations ranged from 28±4030 mg Zn/kg dm and 5±234 mg Cu/kg dm,
with laying hen feeds generally having higher heavy metal contents than broiler feeds. Concentrations of Zn and Cu in dairy and
beef cattle feeds were much lower than in pig and poultry feeds. Pig manures typically contained c.500 mg Zn/kg dm and c.360
mg Cu/kg dm, re¯ecting metal concentrations in the feeds. Typical concentrations in poultry manures were c.400 mg Zn/kg dm
and c.80 mg Cu/kg dm, and in cattle manures c.180 mg Zn/kg dm and c.50 mg Cu/kg dm. The dry matter content of cattle and
pig slurries was a useful indicator of heavy metal concentrations on a fresh weight basis. Ó 1999 Elsevier Science Ltd. All rights
reserved.
Keywords: Heavy metals; Livestock feeds; Animal manures
1. Introduction
The soil acts as a long-term sink for heavy metals,
which can have residence times ranging from hundreds
to thousands of years depending on the element and the
properties of the soil (Alloway, 1995). In view of the
potential long-term impacts of heavy metals on soil
fertility and proposed EC legislation on cadmium and
lead concentrations in food raw materials, it is important to quantify metal inputs to agricultural soils and
assess which soils are most vulnerable to heavy metal
pollution, so that they can be managed appropriately to
reduce potential risks. One approach to assessing the
impact of agricultural management practices on the
heavy metal content of soils is to construct balances or
budgets. However, these require information on the
quantities of heavy metals which are input to and lost
from the agricultural systems under consideration.
*
Corresponding author.
The major routes of heavy metal inputs to agricultural soils include atmospheric deposition, sewage
sludge, animal manures, agrochemicals and inorganic
fertilisers (Nicholson et al., 1998). Losses occur through
o€take in crops or livestock products, leaching and soil
erosion. Whilst other researchers have considered in
some detail metal inputs to soils via sewage sludge,
inorganic fertilisers and atmospheric deposition (Alloway, 1995; Smith, 1996), there has to date been little
information available on heavy metal inputs via animal
manures (cattle, poultry and pigs) in England and
Wales.
In this study, the heavy metal contents of a range of
farm manures were measured to determine mean concentrations for each manure type, so that more accurate metal budgets could be constructed and `typical'
rates of heavy metal inputs to agricultural land could
be calculated. Because the metals present in animal
manures are largely derived from feeds, this study also
sought to assess the heavy metal contents of livestock
feeds used on the farms visited to collect the manure
samples.
0960-8524/99/$ ± see front matter Ó 1999 Elsevier Science Ltd. All rights reserved.
PII: S 0 9 6 0 - 8 5 2 4 ( 9 9 ) 0 0 0 1 7 - 6
24
F.A. Nicholson et al. / Bioresource Technology 70 (1999) 23±31
2. Methods
3. Results
2.1. Sample collection
3.1. Heavy metal contents of livestock feeds
Samples of compound, home-mixed and mill-mixed
feeds were collected direct from the bags or hopper duct.
Where available, the individual ingredients used in
home- or mill-mixed formulations were sampled directly, and details of the proportions used in the mix recorded.
Feed samples were collected by taking 20 individual
samples and bulking these together to provide one
sample of 5±10 kg (solids) or 10±20 l (liquids) for
analysis. A total of 183 feed samples were collected.
Slurry samples were collected by taking ®ve subsamples from di€erent positions in the slurry stores. The
sub-samples were bulked, thoroughly mixed and transferred to polythene containers. Approximately 30 l of
slurry was obtained from each site. Straw-based farmyard manures from both cattle and pig units (FYM),
and poultry manure samples were collected by ®rst removing surface-weathered manure from 10 points on
the manure heaps. At each point, a hole approximately
0.5 m deep was dug into the heap, and several small grab
handfuls of unweathered manure taken from each hole.
These were placed on a tray, the lumps broken up by
hand and then thoroughly mixed before being transferred into polythene bags. Approximately 30 kg of
FYM/poultry manure was collected as appropriate from
each site visited.
Care was taken to ensure that the slurries were well
agitated prior to collection and that the manure samples
were representative of a particular animal type/breeding
system. All manures were stored in a cool environment
(c.4°C) prior to analysis. A total of 85 manure samples
were collected, the number and type being intended to
re¯ect the relative quantities of manure produced from
each farming system.
Results of the feed sample analyses on a dry matter
basis are summarised by livestock type in Tables 1±3.
Concentrations of Hg are not reported here as values
were <0.10 mg/kg dm for nearly all samples.
The highest metal concentrations in dairy cattle feeds
were for Zn and Cu, with typical concentrations in dairy
cake/nuts of c.130 mg Zn/kg dm and c.40 mg Cu/kg dm
(Table 1). Mineral supplements given to dairy cattle had
higher concentrations of Zn (mean c.2900 mg/kg dm)
and Cu (mean c.1500 mg/kg dm). Mineral supplements
also contained higher concentrations of Ni, Pb, Cd, As
and Cr than did other feed components.
The highest metal concentrations in beef cattle feeds
were again for Zn and Cu, with typical concentrations in
beef cake/nuts of c.190 mg Zn/kg dm and c.35 mg Cu/kg
dm (Table 1), similar to levels in the equivalent dairy
feeds. Grass silage, hay and straw fed to both beef and
dairy cattle contained c.30 mg Zn/kg dm and c.6 mg Cu/
kg dm. Concentrations of Ni, Pb, Cd, As and Cr in all
feedstu€s (except minerals) given to dairy and beef cattle
were <5 mg/kg dm.
Concentrations of Zn and Cu in compound and
home-mix pig feeds were higher than in most cattle feeds
(Table 2). Rearer creep feeds (fed to pigs of <10 kg
liveweight) had the highest concentrations of Zn (c.2300
mg/kg dm) and Cu (c.175 mg/kg dm), although these
concentrations decreased through the rearer feeding cycle to c.250 mg Zn/kg dm and c.120 mg Cu/kg dm for
rearer ®nisher rations (fed to pigs from 30 to 90 kg
liveweight). Sow feeds typically had lower concentrations
of Zn and Cu (c.175 mg Zn/kg dm and c.50 mg Cu/kg
dm). There was, however, wide variation in Zn concentrations, particularly in the rearer feeds (range 173±2920
mg/kg dm). Concentrations of Ni, Pb, Cd, As and Cr
were typically <5 mg/kg dm in all the compound and
home-mix pig feeds analysed. Only one mineral supplement was collected and this had relatively high concentrations of Pb (12.9 mg/kg dm) and Cr (18.6 mg/kg dm),
in addition to 3870 mg Zn/kg dm and 7290 mg Cu/kg dm.
Concentrations of Zn in compound poultry feeds were
typically in the range 100±200 mg/kg dm, whilst Cu
concentrations ranged from 20±50 mg/kg dm (Table 3).
Concentrations of Ni, Pb, Cd, As, and Cr were <5 mg/kg
dm in all the compound feeds analysed. Metal concentrations in the home-mix and individual feeds were much
more variable. The layer home-mix feeds generally had
similar Zn and Cu concentrations to the compound feeds,
although one sample had high Zn (4030 mg/kg dm) and
Cu (234 mg/kg dm) concentrations, probably due to excess mineral supplement addition. This sample also had
an unusually high level of Pb (21 mg/kg dm). The cereal
and other plant-derived feeds (soya and sun¯ower meal)
2.2. Sample analysis
The dry matter (DM) content was determined for all
feed and manure samples according to standard methods (MAFF, 1986).
A 300 g (fresh weight) subsample of each solid and
liquid feed was dried and milled. The dried material
(3 g) was analysed for total heavy metals (Zn, Cu, Ni,
Pb, Cd, As, Cr, Hg) by aqua-regia digestion and analysis using inductively coupled plasma spectrophotometry (ICP) or graphite furnace atomic absorption
spectrophotometry (GFAAS). Total heavy metal concentrations in the slurry and solid manure samples were
determined by digesting 100 and 200 g (fresh weight)
subsamples with aqua regia and analysing as above
(MAFF, 1986).
F.A. Nicholson et al. / Bioresource Technology 70 (1999) 23±31
25
Table 1
Dry matter and heavy metal contents of cattle feeds
Feed type
(No. of samples)
Dairy cattle feeds
Dairy cake/nuts (15)
Maize gluten (6)
Molasses (4)
Sugar beet pulp (3)
Minerals (5)
Cereals (1)
Grass silage (18)
Maize silage (2)
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Beef cattle feeds
Beef cake/nuts/pellets Mean
(9)
Range
Rolled oats and barley Mean
(4)
Range
Hay (2)
Mean
Range
Straw (4)
Mean
Range
Grass silage (10)
Mean
Range
Dry matter
(%)
Zn
Cu
Ni
Pb
(mg/kg dm)
Cd
As
Cr
86.2
84.5±87.9
86.2
85.1±87.6
63.9
60.7±67.8
87.0
86.9±87.0
96.7
95.4±98.0
86.2
28.9
18.6±41.4
28.6
27.6±29.6
129
39±289
91
64±192
26
23±32
27
21±32
2900
1540±4530
26
30
21±48
29
28±30
42.2
10.6±76.9
10.2
3.9±35.6
9.3
5.7±15.0
4.6
3.2±6.1
1484
909±2500
6.9
6.2
3.2±9.9
4.2
2.8±5.7
2.8
0.6±7.2
1.6
0.8±3.6
1.2
0.3±2.1
2.5
1.3±4.0
9.0
7.3±11.2
<1.00
0.8
0.1±2.0
4.3
0.4±8.2
2.00
<1.00±5.18
2.07
<1.00±3.51
2.24
<1.00±5.28
2.24
<1.00±3.54
5.50
3.33±8.23
1.88
<1.00
<1.00±3.97
<1.00
<1.00
0.19
<0.10±0.41
0.12
<0.10±0.21
<0.10
<0.10
0.29
0.2±0.4
1.79
0.36±3.59
<0.10
<0.10
<0.10±0.15
0.16
<0.10±0.27
0.37
0.1±0.87
0.13
<0.10±0.28
0.20
<0.10±0.29
1.06
0.87±1.26
3.03
1.26±4.13
0.11
0.10
<0.10±0.15
<0.10
<0.10
2.07
0.6±3.94
1.27
0.71±2.47
0.66
<0.20±1.12
1.77
0.52±2.90
42.0
18.1±53.8
0.26
0.21
<0.20±0.75
1.90
<0.20±3.75
86.3
189
34.6
3.1
<1.00
0.27
0.49
1.66
84.9±88.8
84.1
56±777
39
5.3±61.5
7.6
2.1±4.3
2.4
<1.00±2.69
1.16
0.10±0.79
<0.10
0.24±1.16
<0.10
0.95±3.06
<0.20
82.3±86.8
83.0
78.2±87.8
88.7
86.9±92.7
35.0
18.3±69.5
22±59
29
17±41
11
43±252
38
26±53
3.7±15.9
6.8
5.0±8.6
3.7
2.0±5.6
7.0
3.3±10.8
0.3±8.3
0.8
0.5±1.1
0.5
0.3±0.7
1.1
0.2±2.5
<1.00±3.14
3.64
2.84±4.43
<1.00
<1.00
1.19
<1.00 ± 4.99
<0.10±0.16
0.11
<0.10±0.17
0.10
<0.10±0.13
0.10
<0.10±0.33
<0.10±0.13
<0.10
<0.10±0.10
<0.10
<0.10±0.19
0.16
<0.10±0.44
<0.20
0.28
<0.20±0.45
<0.20
<0.20±0.33
0.47
<0.20±2.09
Note: Where samples were below the limit of detection (LOD), a value of 0.5 ´ LOD was used to calculate means.
had relatively low concentrations of all metals. Limestone
and ®shmeal, which are added to feeds to strengthen egg
shells and bones, generally had low concentrations of Zn
(c.90 mg/kg dm) and Cu (c.10 mg/kg dm), although one
sample of limestone contained high levels of these metals
(3020 mg Zn/kg dm and 527 mg Cu/kg dm). The limestone also contained a relatively high concentration of Pb
(c.10 mg/kg dm). Dicalcium phosphate, another shell and
bone strengthener, had relatively high levels of Zn (375
mg/kg dm) and Cr (118.5 mg/kg dm).
3.2. Heavy metal contents of animal manures
Results of the farm manure analyses on a dry matter
(mg/kg) basis are presented for each livestock type in
Table 4. Concentrations of Hg are not reported as values were <0.05 mg/kg dm in all manure samples.
Concentrations of Zn (c.180 mg/kg dm) and Cu (c.50
mg/kg dm) in dairy cattle manures were generally higher
than in beef cattle manures, which contained c.110 mg
Zn/kg dm and c. 25 mg Cu/kg dm. These di€erences
were most likely due to mineral supplements fed to dairy
cattle which were enriched with these metals. Of the
three dairy farms which supplied minerals for analysis,
one of the corresponding slurry samples had elevated
concentrations of both Zn and Cu, while one had elevated levels of Zn only. For both dairy and beef cattle
manures, concentrations of all the metals tended to be
higher in slurries than in FYM; however, concentrations
of Ni, Pb, Cd, As, and Cr were typically <20 mg/kg dm
in both slurry and FYM.
Higher concentrations of Zn and Cu were found in
pig manures than in dairy or beef cattle manures. Mean
concentrations in pig manures were c.500 mg Zn/kg dm
and c.360 mg Cu/kg dm. Concentrations of the other
metals (Ni, Pb, Cd, As and Cr) were usually <5 mg/kg
dm, although Ni concentrations of >10 mg/kg dm were
found in several slurry samples. The high Zn and Cu
concentrations measured in pig manures are a re¯ection
of metal concentrations in the feeds given to rearer
pigs. In general, manures from farms where the feeds
contained higher concentrations of Cu also had higher
Cu concentrations in the manures. There were samples
of compound and home-mix rearer creep feeds which
had >2500 mg Zn/kg dm, however, only two of the
corresponding pig slurry samples and one of the pig
FYM samples, contained greater than the average
amount of Zn. The pig slurry which contained the
26
F.A. Nicholson et al. / Bioresource Technology 70 (1999) 23±31
Table 2
Dry matter and heavy metal contents of compound and home-mix pig feeds
Feed type (No. of samples)
Dry matter Zn
(%)
Cu
Ni
Pb
(mg/kg dm)
Cd
As
Cr
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
89.8
88.0±91.4
87.7
86.1±90.2
87.8
87.3±88.3
87.9
87.2±88.5
86.9
85.4±87.7
87.7
86.1±89.1
2194
216±2920
834
212±2350
356
193±914
308
173±986
177
158±198
232
150±388
185
150±214
161
121±190
159
84.8±217
128
89.6±183
28.5
20.9±34.3
31.1
17.9±45.5
2.3
2.2±2.6
2.3
2.0±2.6
3.1
1.7±3.5
2.8
1.2±4.3
2.7
2.0±3.7
1.2
0.4± 2.1
<1.00
<1.00
<1.00
<1.00±1.40
<1.00
<1.00
<1.00
<1.00±1.52
<1.00
<1.00
2.10
<1.00±3.19
0.18
0.10±0.29
0.13
0.11±0.14
<0.10
<0.10±0.19
<0.10
<0.10±0.15
0.16
0.13±0.20
<0.10
<0.10±0.11
0.36
0.19±0.72
0.43
0.29±0.58
0.39
0.13±1.07
0.28
0.10±0.63
0.38
0.14±0.78
0.39
0.13±0.81
0.35
<0.20±0.86
0.75
0.05±1.33
0.54
<0.20±1.13
0.80
<0.20±1.17
1.31
1.17±1.59
0.81
<0.20±1.39
Mean
Range
Rearer-®nisher (3)
Mean
Range
Sow-dry and lactating (4) Mean
Range
Soya (1)
Fishmeal (1)
Minerals (1)
88.7
88.0
87.8±88.3
87.9
87.8±88.0
86.6
83.4±87.9
86.9
91.9
97.0
2580
145
99.8±169
144
102±187
129
118±152
67
83
3870
147
166
159±172
89.8
79.4±105
91.7
17.3±160
21.3
4.5
7290
1.6
3.3
1.8±4.6
2.6
1.3±3.4
3.7
1.6±5.9
5.9
1.7
4.5
1.20
<1.00
<1.00
<1.00
<1.00±1.90
<1.00
<1.00±2.42
<1.00
2.22
12.90
0.25
<0.10
<0.10±0.14
<0.10
<0.10±0.17
0.13
0.10±0.15
0.14
0.57
0.80
0.25
0.31
0.15±0.56
0.11
<0.10±0.16
0.15
<0.10±0.28
<0.10
2.39
2.03
0.21
0.38
<0.20±0.77
0.77
0.71±0.81
0.85
0.30±1.30
0.30
<0.20
18.60
Compound feeds
Rearer-creep (4)
Rearer-weaner (4)
Rearer-grower (5)
Rearer-®nisher (7)
Sow-dry (3)
Sow-lactating (3)
Home-mix feeds and
ingredients
Rearer-creep (1)
Rearer-grower (3)
Note: Where samples were below the limit of detection (LOD), a value of 0.5 ´ LOD was used to calculate means.
highest amount of Ni (49.8 mg/kg dm) was from a farm
which provided a sample of feed which also had a high
Ni content (36.6 mg/kg dm), although there were not
enough feed samples high in Ni to con®rm this as a
general pattern.
Typical Zn concentrations in poultry manures were
c.400 mg/kg dm, similar to those found in pig manures,
but concentrations of Cu were considerably lower (c.80
mg/kg dm). Units which supplied samples of mineral
and broiler-breeder supplements with high Zn (>4000
mg/kg dm) and Cu (>600 mg/kg dm) levels, did not have
greater than average Zn or Cu concentrations in the
manure. Zn and Cu concentrations were 2±5 times
higher in poultry manures than in poultry feeds, re¯ecting the eciency of feed conversion by the birds
compared with cattle, where feed and manure metal
concentrations were very similar. Concentrations of Ni,
Pb, Cd, As and Cr were generally <10 mg/kg dm in
poultry manures. However, relatively high levels of Cr
(c.70 mg/kg dm) and As (c.40 mg/kg dm) were observed
in two broiler/turkey litter samples. One was from a unit
where correspondingly high amounts of these metals
were found in two of the feed samples, although there
was no indication of high levels of Cr and As in feeds
from the other unit. There was no obvious explanation
of why these particular feeds had elevated levels of these
two metals.
4. Discussion
4.1. Heavy metals in livestock feeds
Zinc (mostly in the form of zinc oxide) is added to pig
rearer feeds as a `cure-all' for scour, and in the UK can
be given to pigs of <10 kg liveweight without a veterinary prescription. For larger pigs a prescription is required, and hence these feeds contain less Zn. Copper
(mostly in the form of copper sulphate) is added to pig
feeds to suppress bacterial action in the gut and to
maximise feed utilisation by the animal. Background
levels of Cu in feedstu€s are considered to be c.30 mg/kg
dm, and permissible addition levels of Cu depend on the
size of the pigs, namely: 175 mg Cu/kg dm for growers
(weight 0±30 kg), 100 mg Cu/kg dm for ®nishers (weight
30±90 kg) and nil for adult sows (weight >90 kg).
In this study, Cu concentrations in the compound pig
feeds generally decreased as the size of the pigs increased
(Table 2). Concentrations of Cu in compound feeds for
sows were close to background levels (c.30 mg/kg dm),
however, in two cases the Cu content of home-mix sow
feed was much higher than this.
The feed Zn and Cu concentrations in this survey
were compared with those reported by McDonald et al.
(1981) and with estimated values for minerals in feeds
from the Netherlands (Jongbloed and Lenis, 1993),
F.A. Nicholson et al. / Bioresource Technology 70 (1999) 23±31
27
Table 3
Dry matter and heavy metal contents of compound and home-mix poultry feeds
Feed type (No. samples)
Compound feeds
Broiler-starter (4)
Broiler-grower (4)
Broiler-®nisher (3)
Turkey-various (6)
Turkey-grower (4)
Turkey-®nisher (3)
Layer (4)
Home-mix feeds and
ingredients
Layer (7)
Cereals (7)
Soya, sun¯ower and
wheat feed (7)
Limestone (5)
Fishmeal (2)
Broiler breeder supplement and minerals (2)
Dry matter
(%)
Zn
Cu
Ni
Pb
(mg/kg dm)
Cd
As
Cr
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
88.8
88.0±89.4
88.5
88.1±89.2
88.5
88.1±89.3
86.6
85.5±88.0
87.2
86.4±87.9
87.3
86.2±88.8
89.0
88.4±89.4
148
124±169
118
106±126
135
126±148
155
107±210
120
105±127
108
102±114
153
94.2±311
31.7
29.0±36.0
36.1
24.8±52.4
32.6
29.8±37.4
27.8
27.8±49.7
26.5
15.3±35.9
19.9
13.2±27.8
23.0
10.7±56.1
2.0
1.1±2.8
2.0
1.3±2.8
2.1
1.1±3.9
1.8
0.7±2.8
2.0
0.8±3.0
1.7
0.9±2.2
2.6
1.3±5.2
<1.00
<1.00±2.40
<1.00
<1.00
<1.00
<1.00
<1.00
<1.00
<1.00
<1.00±1.78
<1.00
<1.00
<1.00
<1.00±1.12
0.19
<0.10±0.33
0.16
<0.10±0.23
0.12
<0.10±0.17
0.15
0.22±0.25
0.14
<0.10±0.20
0.19
0.17±0.21
0.39
0.32±0.46
0.23
0.17±0.31
0.25
0.18±0.31
0.15
0.14±0.16
0.35
0.22±0.57
0.28
<0.10±0.52
<0.10
<0.10±0.16
<0.10
<0.10±0.18
1.77
0.65±3.44
1.44
0.49±3.42
0.22
<0.20±0.56
2.08
0.76±3.17
1.13
0.21±2.24
0.72
0.60±0.88
0.76
0.34±1.35
Mean
Range
Mean
Range
Mean
89.8
86.6±99.1
87.7
86.1±90.1
88.6
636
27.6±4030
29
23.7±46.1
66.0
43.1
4.5±234
4.6
3.5±6.6
17.0
1.7
0.1±3.3
0.4
0.1±1.1
5.1
4.85
<1.00±20.60
1.34
<1.00±5.10
1.17
0.55
<0.10±2.27
0.15
<0.10±0.37
0.17
0.21
<0.10±0.95
<0.10
<0.10
0.06
0.84
<0.20±1.96
0.78
<0.20±3.86
0.32
Range
Mean
Range
Mean
Range
Mean
86.7±91.5
99.9
99.7±100.0
91.5
91.4±91.6
96.8
41.2±95.0
620
7.6±3020
92.8
92.2±93.3
6980
14.2±22.9
107
<1.0±527
4.8
2.7±6.9
887
2.1±9.9
0.9
0.3±2.2
1.6
0.1±3.2
4.4
<1.00±3.24
9.79
3.99±14.90
2.06
1.79±2.33
10.50
<0.10±0.80
2.56
0.46±4.40
0.50
0.22±0.78
1.66
<0.10±0.10
0.46
0.38±0.57
1.30
0.61±1.99
1.27
<0.20±0.80
3.42
1.76±5.09
0.47
0.36±0.58
1.81
95.5±98.1
89.2
88.1±90.2
4190±9370
375
354±396
634±1140
23.2
21.1±25.3
3.0±5.7
2.4
2.0±2.8
3.4±17.60
2.26
1.52±2.99
0.96±2.35
1.53
1.35±1.70
1.12±1.41
4.17
3.91±4.42
1.31±2.30
119
110±127
Range
Dicalcium phosphate (2) Mean
Range
Note: Where samples were below the limit of detection (LOD), a value of 0.5 ´ LOD was used to calculate means.
(Table 5). Agreement was good between the results of
this survey and that of McDonald et al. (1981) for the
Zn and Cu contents of silage, straw, hay, sugar beet,
cereals, soya and ®shmeal. However, Zn concentrations
in most of the pig and poultry feeds in this survey were
much higher than those estimated by Jongbloed and
Lenis (1993). Also Cu concentrations in some of the pig
rearer and poultry layer feeds were higher than those
estimated by the Dutch authors, probably because of
tighter restrictions on Cu additions in the Netherlands.
Whilst Zn is needed by poultry for growth, feather
and skeletal development, and reproduction (Bolton and
Blair, 1974), the amount required is only c.50 mg/kg dm
(ARC, 1975). This suggests that current Zn concentrations of some compound poultry feeds are 2±3 times
higher than that required by the birds for healthy development, and that consideration should be given to
reducing levels. Current Cu concentrations in compound poultry feeds are at background levels (c.30 mg/
kg dm), which is adequate to meet poultry Cu requirements of c.4 mg/kg dm (ARC, 1975).
4.2. Heavy metals in animal manures
The heavy metal contents of farm manures are largely
a re¯ection of their concentrations in the feeds consumed and the eciency of feed conversion by the animals. Fleming and Mordenti (1991) reported mean Zn
concentrations in Belgian cattle manures of 580 mg/kg
dm. However, both this study and a survey of Swiss
manures (Menzi and Kessler, 1998) generally found
<200 mg Zn/kg dm in cattle manures. A previous review
of manure metal concentrations (Webber and Webber,
1983) also reported cattle manure Zn concentrations in
the range 30±225 mg/kg dm. Cu concentrations in cattle
manures were similar in all three studies at c.60 mg/kg
dm (Fleming and Mordenti, 1991), median values in the
range 19±53 mg/kg dm (Menzi and Kessler, 1998) and
mean values in the range 16±62 mg/kg dm (this study).
Menzi and Kessler (1998) found slightly lower mean Cd
and Pb concentrations than the present study at c.0.17
mg Cd/kg dm (this study c.0.28 mg Cd/kg dm) and c.3.0
mg Pb/kg dm (this study c.4.6 mg Pb/kg dm).
28
F.A. Nicholson et al. / Bioresource Technology 70 (1999) 23±31
Table 4
Dry matter and heavy metal contents of animal manures
Manure type
(No. of samples)
Dry matter
(%)
Zn
Cu
Ni
Pb
(mg/kg dm)
Cd
As
Cr
Dairy cattle FYM (6)
18.4
14.9±30.1
7.6
0.2±16.1
21.0
16.4±24.2
12.0
2.2±21.0
21.7
14.4±32.6
4.4
0.5±21.6
59.3
46.0±78.0
40.7
23.0±67.1
153
99±238
209
<5±727
81
41±274
133
68±235
431
206±716
575
<5±2500
378
208±473
459
350±632
37.5
26.2±55.8
62.3
<1.0±352
16.4
10.5±27.9
33.2
17.5±48.7
374
160±780
351
<1.0±807
96.8
45.7±173
64.8
49.4±74.8
3.7
1.7±9.1
5.4
0.1±11.4
2.0
0.2±3.1
6.4
1.9±20.4
7.5
3.0±24.3
10.4
<0.1±49.8
5.4
2.2±12.3
7.1
4.5±11.4
3.61
<1.00±9.18
5.87
<1.00±16.9
1.95
<1.00±6.40
7.07
1.07±18.0
2.94
1.01±4.65
2.48
<1.00±9.74
3.62
<1.00±9.28
8.37
3.36±14.80
0.38
<0.10±0.53
0.33
<0.10±1.74
0.13
<0.10±0.24
0.26
0.11±0.53
0.37
0.19±0.53
0.30
<0.10±0.84
0.42
0.20±1.16
1.06
0.44±2.04
1.63
0.57±4.83
1.44
<0.10±4.48
0.79
0.39±1.53
2.60
0.43±10.8
0.86
0.52±1.34
1.68
<0.10±6.7
9.01
<0.10±41.1
0.46
0.15±0.82
5.32
0.77±21.40
5.64
<0.20±12.9
1.41
0.79±2.05
4.69
1.13±15.7
1.98
0.67±3.42
2.82
<0.20±6.81
17.17
3.57±79.8
4.57
2.14±7.06
Mean
Range
Dairy cattle slurry (20) Mean
Range
Beef cattle FYM (12)
Mean
Range
Beef cattle slurry (8)
Mean
Range
Pig FYM (7)
Mean
Range
Pig slurry (12)
Mean
Range
Broiler/turkey litter (12) Mean
Range
Layer manure (8)
Mean
Range
Note: Where samples were below the limit of detection (LOD), a value of 0.5 ´ LOD was used to calculate means.
Table 5
Review of Zn and Cu concentrations in animal feeds
Feed type
Zn (mg/kg dm)
Cu (mg/kg dm)
Source
This study
Other
This study
Other
Pig starter feed
Pig weaner feed
Pig grower feed
Pig ®nishing feed
Sow lactating feed
Sow dry feed
Broiler feed
Layer feed (compound)
Layer feed (home-mix)
216±2920
212±2350
193±914
173±986
150±388
158±198
106±169
94±311
28±4030
100
100
90
90
75
75
90
90
90
150±214
121±190
85±217
90±198
18±46
21±34
25±52
11±56
5±234
175
175
35
35
35
35
25
20
20
1
1
1
1
1
1
1
1
1
Grass silage
Straw
Hay
Sugar beet pulp
Oats and barley
Soya
Fishmeal
21±53
6±18
17±41
21±32
22±59
67
83
33
16±29
n/a
32
28
30
119
3.2±9.9
2.0±5.6
5.0±8.6
3.2±6.1
3.7±15.9
21.3
4.5
8.0
2.2±2.8
7.3±13.4
25
2.9±7.6
24.2
5.1
2
2
2
2
2
2
2
Source: (1) Jongbloed and Lenis (1993), (2) McDonald et al. (1981).
A number of authors have measured Zn and Cu
concentrations in pig manures. For example, the following Zn concentrations have been reported: 150 mg/
kg dm (Berryman, 1971), 595 mg/kg dm (Kornegay
et al., 1976), 128±981 mg/kg dm (Webber and Webber,
1983), 919 mg/kg dm (Fleming and Mordenti, 1991),
554±747 mg/kg dm (Menzi and Kessler, 1998). Similarly,
Cu concentrations of 675 mg/kg dm (Berryman, 1971),
869 mg/kg dm (Kornegay et al., 1976), 22±1575 mg/kg
dm (Webber and Webber, 1983), 574 mg/kg dm (Fleming and Mordenti, 1991) and 71±119 mg/kg dm (Menzi
and Kessler, 1998) have been reported. These ranges,
like those found in the present study, are extremely
broad and clearly dependent to a large extent on the age
of the pigs and the quantities of Zn or Cu supplements
added to the diet. Menzi and Kessler (1998) reported
similar Cd and Pb concentrations to those found in this
study at c.0.20 mg Cd/kg dm (this study c.0.34 mg Cd/kg
dm) and c.2.3 mg Pb/kg dm (this study c.2.4 mg Pb/kg
dm).
The heavy metal contents of poultry manures have
previously been shown to be related to additions in the
diet. For example, Kunkle et al. (1981) showed that Cu
levels in broiler litter were linearly related to Cu added
in the diet and were concentrated 3.25 times. Similarly,
Morrison (1969) found that As additions to the diet
resulted in a sevenfold increase in As concentrations in
broiler litter. Whilst the type of material (eg. woodchips,
straw) used for broiler bedding may in¯uence litter dry
matter and other chemical properties, it has little e€ect
F.A. Nicholson et al. / Bioresource Technology 70 (1999) 23±31
on the heavy metal concentrations of the resulting litter.
Typically, for broilers c.30% of the litter is bedding
material (MAFF, 1994), which has heavy metal
concentrations at background levels for plant material
(F. A. Nicholson, unpublished data).
In a comprehensive review of heavy metal levels in
poultry manures, Sims and Wolf (1994) summarised
®ndings from previous research projects carried out
between 1969 and 1992. Zn concentrations ranged from
non-detectable (nd) to 660 mg/kg dm in poultry manure
(this study c.460 mg/kg dm) and from nd to 669 mg/kg
dm in poultry litter (this study c.380 mg/kg dm). Cu
concentrations in poultry manures were in the range nd
± 232 mg/kg dm (this study c.65 mg/kg dm) and in
poultry litters nd ± 1003 mg/kg dm (this study c.100 mg/
kg dm), the high Cu concentrations in some of the
manures being ascribed to copper sulphate supplements
added to the diet. Indeed, Cu concentrations in Belgian
poultry manures were found to average only 59 mg/kg
dm (Fleming and Mordenti, 1991), similar to concentrations found in this study. Median Zn and Cu
concentrations in Swiss poultry manures were 349±511
mg/kg dm and 35±44 mg/kg dm, respectively (Menzi and
Kessler, 1998). Concentrations of the other heavy metals
measured in this study were within the ranges reported
by Sims and Wolf (1994) and Fleming and Mordenti
(1991), although Cd and Pb concentrations in
Swiss poultry manures were lower than those found
here at c.0.27 mg/kg dm (this study c.0.74 mg/kg dm)
and c.2.5 mg/kg dm (this study c.6.0 mg/kg dm),
respectively.
29
following linear regression equations were derived from
the data.
Cattle slurries (28 samples)
Total Zn (g/m3 fw)
ˆ (1.58 ´ DM) + 0.89
Total Cu (g/m3 fw)
ˆ (0.37 ´ DM) + 0.84
Total Ni (g/m3 fw)
ˆ (0.07 ´ DM) + 0.06
Total Pb (g/m3 fw)
ˆ (0.08 ´ DM) ÿ 0.13
Total Cd (g/m3 fw)
ˆ (0.003 ´ DM) ÿ 0.002
Total As (g/m3 fw)
ˆ (0.03 ´ DM) ÿ 0.08
Total Cr (g/m3 fw)
ˆ (0.06 ´ DM) ÿ 0.01
(r2 ˆ 66%, p < 0.001)
(r2 ˆ 58%, p < 0.001)
(r2 ˆ 32%, p < 0.05)
(r2 ˆ 47%, p <0.001)
(r2 ˆ 16%, p < 0.05)
(r2 ˆ 22%, p < 0.05)
(r2 ˆ 32%, p < 0.05)
Pig slurries (12 samples)
Total Zn (g/m3 fw)
ˆ (5.46 ´ DM) + 9.99
Total Cu (g/m3 fw)
ˆ (4.61 ´ DM) + 0.71
Total Ni (g/m3 fw)
ˆ (0.14 ´ DM) ÿ 0.003
Total Pb (g/m3 fw)
ˆ (0.10 ´ DM) ÿ 0.21
Total Cd (g/m3 fw)
ˆ (0.004 ´ DM) + 0.002
Total As (g/m3 fw)
ˆ (0.02 ´ DM) ÿ 0.003
Total Cr (g/m3 fw)
ˆ (0.06 ´ DM) ÿ 0.06
4.3. Predicting the heavy metal content of animal manures
The dry matter content of liquid manure samples
(cattle and pig slurries) was shown to be a good
predictor of heavy metal concentrations expressed on a
fresh weight (fw) basis, indicating that the heavy metals
are primarily associated with the dry matter component
of slurries rather than being in solution. The
(r2 ˆ 34%, p <0.05)
(r2 ˆ 90%, p < 0.001)
(r2 ˆ 68%, p < 0.001)
(r2 ˆ 96%, p < 0.001)
(r2 ˆ 74%, p < 0.001)
(r2 ˆ 75%, p < 0.001)
(r2 ˆ 98%, p < 0.001)
These relationships can be used to provide an indication
of the likely heavy metal concentrations of slurries from
a knowledge of dry matter contents, where laboratory
heavy metal analysis data are not available.
Table 6
Estimated heavy metal concentrations of `typical' manures and heavy metal loading rates from animal manures applied at 250 kg/ha total N
Manure type
Cattle FYM
Pig FYM
Dairy slurry
Beef slurry
Pig slurry
Broiler/turkey
litter
Layer manure
a
b
Dry
matter
content
(%) a
Total N Concentration
(kg/t
Zn
Cu
Ni
or m3 ) b
25
25
10
10
10
60
6.0
7.0
4.5
3.5
7.0
29
17
60
17
17
65
130
4.0
42
4.5
4.5
47
19
30
15
175
27
Loading rate
Pb
Cr
(g/t or m3 )
As
Cd
Zn
Cu
Ni
Pb
Cr
(kg/ha)
As
Cd
0.7
1.3
0.6
0.6
1.4
2.4
0.6
0.8
0.7
0.7
0.8
2.0
0.5
0.6
0.6
0.6
0.7
1.2
0.3
0.2
0.2
0.2
0.2
0.3
0.06
0.06
0.03
0.03
0.04
0.33
0.7
2.1
0.9
1.2
2.3
1.1
0.2
1.5
0.3
0.3
1.7
0.2
0.03
0.05
0.03
0.04
0.05
0.02
0.03
0.03
0.04
0.05
0.03
0.02
0.02
0.02
0.03
0.04
0.02
0.01
0.01
0.01
0.01
0.02
0.01
<0.01
0.003
0.002
0.002
0.002
0.001
0.003
3.0
2.7
1.7
0.1
0.39
2.9
0.5
0.05
0.05
0.03
<0.01 0.007
Typical dry matter content of manure (MAFF, 1994).
Typical total N content of manure (MAFF, 1994).
30
F.A. Nicholson et al. / Bioresource Technology 70 (1999) 23±31
4.4. Heavy metal loadings from animal manures
Farm manures are a valuable source of major plant
nutrients and organic matter. However, care must be
taken to ensure that manure applications containing
elevated levels of heavy metals do not cause long-term
soil contamination. We therefore calculated the typical
amounts of heavy metals added to soils, where
manures were applied at rates supplying 250 kg total
N/ha per annum in accordance with the maximum
recommended application rate in the Code of Good
Agricultural Practice for the Protection of Water
(MAFF, 1991).
The dry matter contents of the pig and cattle slurries
analysed in the survey ranged from <1 to >20% (Table 4), re¯ecting the e€ect on slurry dry matter of different production systems and storage practices.
However, this survey also found signi®cant relationships between slurry dry matter contents and freshweight metal concentrations. Therefore, to calculate
`typical' metal application rates from slurry applications, it was necessary to use the survey-derived relationships to estimate the heavy metal concentrations of
`typical' undiluted pig and cattle farm slurries with dry
matter contents of c.10% (MAFF, 1994). For example,
cattle slurry with a dry matter content of 10% will
typically have a Zn concentration of 17 g/m3 fw,
whereas pig slurry of the same dry matter content will
have a Zn concentration of 65 g/m3 fw (Table 6). Similarly, the dry matter contents of the solid manures in
the survey varied (Table 4) due to di€erences in the
proportion of straw or woodchips used. Again, it was
necessary to estimate the metal concentrations of `typical' solid manures before metal application rates could
be calculated. This was accomplished using standard
rates of straw (cattle and pig FYM) or woodchip
(broiler/turkey litter) additions to excreta (MAFF,
1994). The metal concentration of cattle/pig excreta was
assumed to be the same as the slurry at 10% dry matter
(Table 6), the metal content of poultry excreta was assumed to be the same as layer manure (Table 6), and the
metal concentrations of straw and woodchips were taken from literature values.
Using the calculated `typical' manure metal concentrations and total nitrogen (N) contents at `typical' dry
matter contents (MAFF, 1994), metal loading rates
from manure applications at 250 kg/ha total N were
estimated (Table 6). Pig FYM and slurry applications at
the rate of 250 kg/ha total N were estimated to apply
c.2.2 kg/ha Zn and c.1.6 kg/ha Cu, and poultry manures
1.1±2.9 kg/ha Zn and 0.2±0.5 kg/ha Cu. Cattle FYM and
slurry dressings typically applied c.1.0 kg/ha Zn and
c.0.3 kg/ha Cu, largely representing the recycling of
metals in the cattle farming system. Estimated Cd addition rates were highest from cattle FYM and broiler/
turkey litter (c.3 g/ha) and from layer manure (c.7 g/ha),
and represented an important source of this metal to
agricultural soils, although Cd is usually thought be
added mainly via atmospheric deposition and phosphate
fertiliser use (Nicholson et al., 1998).
It is important to be aware that heavy metal addition
rates to soils may be greater or less than the `typical'
values given here, depending on the analysis of the
manure and the rate of application. In areas where animal manures (especially pig and poultry manures) have
been applied for many years and where applications are
expected to continue, it is likely that soil heavy metal
accumulation rates (particularly Zn and Cu) will be at
their greatest.
Acknowledgements
Funding of this work from the Ministry of Agriculture Fisheries and Food is gratefully acknowledged.
The authors would also like to thank the ADAS Laboratories at Wolverhampton for sample analysis, and
Mark Silver, Albert Williams, Bob Jackson, Claire
Hurst, Peter Burton and Dr. David Chadwick (IGER,
North Wyke) for managing the sample collection programme.
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