Page 1
Heavy Metal Transfers Between Trophic Compartmentsin Different Ecosystems in Galicia (Northwest Spain):Essential Elements
X. I. Gonzalez Æ J. R. Aboal Æ J. A. Fernandez ÆA. Carballeira
Received: 26 July 2007 / Accepted: 19 February 2008 / Published online: 19 March 2008
� Springer Science+Business Media, LLC 2008
Abstract In the present study, we determined the con-
centrations of Cu, Fe, Mn, and Zn in soil and several
trophic compartments at a total of 16 sampling stations.
The trophic compartments studied were primary pro-
ducers, represented by two species of terrestrial mosses
(Pseudoescleropodium purum and Hypnum cupressiforme)
and oak trees (Quercus robur or Q. pyrenaica); primary
consumers, represented by the wood mouse (Apodemus
sylvaticus) and the yellow necked mouse (A. flavicollis);
secondary consumers, represented by the shrew (Sorex
granarius); and finally, detritivores, represented by slugs
(Arion ater). Thirteen of the sampling stations were located
in mature oak woodlands (Quercus sp.); two of the sam-
pling stations were located in the area surrounding a
restored lignite mine dump, and the other in an ultrabasic
area. The analytical determinations revealed a lack of
significant correlations among trophic compartments, pos-
sibly caused by effective regulation of metals by organisms
and/or spatial variation in availability of metals from soil
or food. Furthermore, the only element that showed a clear
pattern of biomagnification was Cu; as for the other ele-
ments, there was always some divergence from such a
pattern. Finally, the patterns of bioaccumulation in con-
taminated and woodland sampling stations were very
similar, although there was enrichment of the concentra-
tions of Cu, Mn, and Zn in the mice viscera, which, except
for Mn, were related to higher edaphic concentrations.
Information about the movement of metals through eco-
systems, as well as their bioaccumulation, trophic transfer,
and potential toxicological effects, is provided by mea-
suring the concentrations in soil and biota. The persistence,
biomagnification, and distribution of trace metals in ter-
restrial food webs have been investigated in many studies
(Roberts and Johnson, 1978; Roberts et al. 1978; Hunter
and Johnson, 1982; Hunter 1984; Hunter et al. 1987a-c;
Beyer et al. 1985; Scanlon, 1987; Scharenberg and Ebeling
1996; Seifert et al. 1999; Milton et al. 2002; Blakbern
2003). Patterns of uptake and bioaccumulation have been
studied by investigating the relationships between metal
concentrations in soils and several parts of plants (Davies
et al. 1987; Otte et al. 1990; Folkeson et al. 1990; Coquery
and Welbourn 1995; Kalas et al. 2000; Mertens et al. 2001;
Nan et al. 2002) and also the relationships between metal
concentration in soils and tissues of co-occurring animals
(Sharma and Shupe 1977; Lubben and Sauerbeck 1991;
Shore 1995; Laurinolli and Bendell-Young 1996; Kalas
et al. 2000; Torres and Johnson 2001; Milton and Johnson
2002; Milton et al. 2003).
The relative concentrations of metals in plant tissues
(Lubben and Sauerbeck 1991) or animals (Hunter and
Johnson 1982; Laurinolli and Bendell-Young 1996) can
reveal general trends of exposure, uptake, translocation,
and assimilation of metals within organisms. Furthermore,
the trophic transfer of metals within the food web can be
demonstrated by relating metal levels in dietary compo-
nents with those assimilated by an animal (Torres and
Johnson 2001).
The bioavailability of heavy metals in soils varies
depending on physical, chemical, and biological factors
(Ross 1994; Ernst 1996; Torres and Johnson 2001), and for
accurate assessment of the potential toxicity of an element
in the environment, analysis of trophic compartments must
X. I. Gonzalez � J. R. Aboal (&) � J. A. Fernandez �A. Carballeira
Area de Ecologıa, Facultad de Biologıa, Universidad de Santiago
de Compostela, 15782 Santiago de Compostela, Spain
e-mail: [email protected]
123
Arch Environ Contam Toxicol (2008) 55:691–700
DOI 10.1007/s00244-008-9157-y
Page 2
be carried out. Organisms respond to the bioavailability of
the pollutants and integrate them in their tissues, and
therefore reliable assessment of the ecological risk can be
achieved by analysis of the biota (Beyer et al. 1990;
Talmage and Walton 1991; Abdul Rida and Bouche 1997).
In this study, we report the concentrations and distribu-
tion of Cu, Fe, Mn, and Zn in several trophic compartments
at a total of 16 sampling stations (SSs). These essential
metals are effectively regulated by homeostasis and are
maintained constant almost irrespective of dietary intake
(Roberts and Johnson 1978; Talmage and Walton 1991).
Three of these SSs were considered polluted sites, and the
remaining SSs were mature and unpolluted woodlands.
At each SS several trophic compartments were sampled:
(i) primary producers, represented here by two species of
terrestrial mosses (Scleropodium purum and Hypnum
cupressiforme) and two species of oak (Quercus robur and
Q. pyrenaica); (ii) primary consumers, represented by mice
(Apodemus sylvaticus and A. flavicollis), and secondary
consumers, represented by shrews (Sorex granarius); and
(iii) finally, detritivorous organisms, represented by slugs
(Arion ater). Furthermore, different inputs to the ecosys-
tems were represented: soil sections as atmospheric and
geochemical inputs, and mosses as atmospheric inputs.
The principal aim of the study was to compare the
contents of Cu, Fe, Mn, and Zn in biota in natural and
anthropogenic ecosystems. A further aim was to try to
demonstrate the uptake of metals by small mammals,
vegetation, and detritivores and to detect the trophic
transfer between compartments by analysis of metallic
concentrations.
Materials and Methods
Description of the Sampling Stations
The location and the area of the 16 SSs selected in Galicia
(northwestern Spain) are shown in Fig. 1. Two SSs were
located in restored mine dumps of a coal-fired power plant:
SS1, of recent origin (2001) and correctly restored, is sit-
uated in an area revegetated with grasses, whereas SS2,
which is older (1987) and badly restored, is situated in a
forest of Castanea sativa, with poorly developed shrub.
SS3 is located in an area of ultrabasic serpentinized rocks
dominated by low-lying shrubs. The remaining SSs (SS4–
SS16), all situated in mature woodland dominated by
Quercus robur, were selected based on three criteria: (i)
area [100 ha; (ii) Quercus robur or Q. pyrenaica as
dominant species ([50% relative abundance), with an
orthogonal projection [80%; and (iii) a ratio of the area
(m2) to the perimeter (m) [100 (to minimize edge effect).
In all cases, the woodlands were far from roads, buildings,
and focal points of pollution. All of the woodlands were
considered the control sites in the present study, although
SS4 to SS6 and SS8 to SS10 are located within a 15- to
35-km radius of the above-mentioned power plant.
Sampling and Sample Processing
Field sampling was carried out during autumn, in 2001
and 2002. Soil samples were collected from two depths:
0–15 cm, to describe atmospheric deposition plus local
geochemistry; and 15–30 cm, to assess the influence of
local geochemistry. For each depth, a total of eight subs-
amples were collected from throughout the study area
(avoiding margins and boundaries) to reduce the spatial
variability of the metals in the soil. The subsamples were
combined to make a composite sample, and plant remains,
stones, etc., were eliminated from the samples in the field.
Before analysis, the soils were dried at room temperature
(20 ± 2�C) and sieved through a 2-mm stainless-steel
mesh. The samples were then ground to a homogeneous
powder in an agate mortar.
At the woodland SSs, samples of oak leaves were also
collected; Quercus robur leaves were collected at all sites
except SS12, SS13, and SS16, at which Q. pyrenaica
leaves were collected (Q. robur does not grow in south-
eastern Galicia). A total of 50 trees were sampled at each
SS throughout the entire area. One branch of approximately
4-cm diameter was cut from each tree at a height of 5 m.
Branches facing the different cardinal points were removed
successively from each tree and the sequence was started
again with the fifth tree. Fifty shaded leaves were collected
from each specimen and were then combined into a com-
posite sample to minimize interindividual variability of
SS7
SS8
SS3
SS14
SS11
SS16
SS12SS13
SS15
SS1
SS2
SS5SS9
SS6
SS10SS4
Spain
50 025 Kilometers
Woodland
Ultrabasic area
Mine dump
(139)
(317)
(254)
(136)(0.3)(1750)
(117)(234)(1339)
(101)
(366)
(101)
(112)
(127)
(3.7)
(581)
Fig. 1 Maps showing the location of Galicia in Spain and the
location and area of the sampling stations in Galicia. Data in
parentheses correspond to the areas expressed as hectares
692 Arch Environ Contam Toxicol (2008) 55:691–700
123
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metal contents (Aboal et al. 2004). The leaves were
cleaned of epiphytic organisms, insect eggs, fungi, and
other debris, then washed in distilled water for 15 min with
shaking, and, finally, homogenized in a laboratory blender
(Waring Laboratory Blendor). The washing was carried out
to eliminate the fraction associated with aerosols from the
surfaces of the leaves, as in the present study we wished to
estimate the ability of both Quercus species to bioaccu-
mulate heavy metals (and not to estimate atmospheric
deposition).
Terrestrial mosses are already known to be suitable for
biomonitoring atmospheric pollution, and have been used
in this way in studies similar to the present study (Kalas
et al. 2000), because the extent of contamination due to
atmospheric deposition can be determined by comparing
the concentrations in the oak samples with those in the
moss samples (Aboal et al. 2004). Pseudoscleropodium
purum was collected at all SSs except SS2, where Hypnum
cupressiforme was collected. At each SS, three gaps were
selected, and at each a total of 30 subsamples were col-
lected (Fernandez et al. 2002; Aboal et al. 2006). The
extreme apices (3–4 cm) of the moss shoots were removed
for analysis to standardize the time of exposure and to
eliminate older tissues. The apical sections were then
rinsed for 30 s in bidistilled water with shaking. Once the
cleaned samples were dried (20�C constant humidity), they
were then homogenized (\100 lm) in an ultracentrifugal
mill (Retsch ZM 100).
At 11 of the SSs (SS4 to SS5 and SS7 to SS15), a
variable number of slugs Arion ater (from 11 to 43 indi-
viduals) were collected by hand. The sampling was carried
out during the early hours of the morning and during the
night (over a period of 6 days), because these animals are
most active at those times. In the laboratory, slugs were
purged for 72 h, by maintaining them (at 10�C) without
food and water to allow passive evacuation of the ali-
mentary tracts. The slugs were placed in clean receptacles
every 24 h to avoid coprophagy and were cleaned of any
adhering feces. After being purged, the slugs were killed by
immersion in distilled water for 24 h, and once dead, they
were cleaned of mucus. All slugs collected at each SS were
chopped in a laboratory blender to form a composite
sample. They were then dried to constant weight at 45�C in
a forced-air oven, then crushed in a porcelain mortar and
homogenized (\100 lm) in an ultracentrifugal mill.
The species of small mammals studied were the wood
mouse Apodemus sylvaticus, an omnivorous species that is
commonly used in monitoring studies (Talmage and Walton
1991), which was collected at all SSs, and the yellow-
necked field mouse Apodemus flavicollis. The latter species
is very similar to A. sylvaticus in ecological and morpho-
logical aspects, and was collected only at SS11, SS14, and
SS16, where both species occurred sympatrically. The
number of specimens of A. sylvaticus collected ranged from
4 to 63, and that of A. flavicollis, from 7 to 19. The period of
sampling was from December 2001 to November 2002; the
samples were collected usually during 5 days except for
SS1 and SS2, for which it was 20 days, and SS4, SS5, and
SS6, for which it was 30 days. The sampling effort, cal-
culated by multiplying the number of traps placed in the
field by the number of days that they remained at each SS,
was between 800 and 900, except for SS3 and SS6, for
which it was 1400, and SS4 and SS5, for which it was 2046.
The traps were arranged on a regular sampling grid spaced
at 10-m intervals (Erry et al. 2000). Mice were captured live
in single and multiple capture traps, placed in equal pro-
portions. All traps were placed a minimum of 30 m from the
borders of the biotope to avoid edge effects, baited with
pieces of bread smeared with peanut butter, and checked
every 24 h. Captured mice were identified, sexed, killed in
the field, and transported on ice (approx. 4�C) to the labo-
ratory. The animals were then frozen at -30�C until
dissection to prevent tissue lysis and redistribution of metals
(Milton and Johnson 2002; Milton et al. 2002, 2003).
Specimens of one insectivorous species, the Spanish
shrew Sorex granarius (which is endemic on the Iberian
Peninsula [Lopez-Fuster 2002]), were captured at nine of
the SSs studied. The sampling period and the sampling
effort were the same as those for Apodemus (see above).
The number of individuals collected ranged from 1 to 15.
Shrews were captured live by multiple-capture and inter-
ception-type traps placed in the same way as for the mice.
Interception-type traps were not baited. The procedure
carried out with shrews was the same as that used for mice,
except that the shrews were identified and sexed in the
laboratory.
The small mammal specimens were defrosted, weighed,
and dissected. Liver, kidneys, and brain of each specimen
were then removed. Dissections were carried out with
stainless-steel dissecting equipment under perfect condi-
tions. As no gender- or age-related differences have been
found for these species (Gonzalez et al. 2008), all organs of
the same type belonging to each species at each SS were
combined to make a composite sample and homogenized
by cutting them into pieces with scissors. About 5 g (w.w.)
of each composite sample was dried to constant weight
(45�C) in a forced-air oven, and once dried, the samples
were ground in a porcelain mortar. The use of composite
sample allows reduction of the intrapopulational variability
associated with the concentrations of the metals (Gonzalez
et al. 2006).
Chemical Analysis
The soil samples (0.5 g) were digested with 10 mL of aqua
regia (3:1 HCl:HNO3, analytical grade), in Teflon bombs in
Arch Environ Contam Toxicol (2008) 55:691–700 693
123
Page 4
a microwave oven (CEM MDS 2100). The soil suspensions
thus obtained were shaken for 5 min and centrifuged at
5000 rpm for 3 min before the supernatant was decanted
off. Approximately 1 g each of mosses and oak leaves and
0.2 g of organs from mice and shrews were digested with
10 mL of HNO3 in Teflon bombs in a microwave oven.
The slug samples (0.6 g) were first digested with 5 mL of
HNO3 and once the reaction bombs had cooled, the sam-
ples were subjected to a second stage of digestion in which
2 mL of H2O2 was added. After the plant samples were
digested, the extracts were clarified by centrifugation
(5000 rpm, 5 min). All extracts were made up to a final
volume of 25 mL. The concentrations of Cu, Fe, Mn, and
Zn were determined by flame absorption spectrophotome-
try (Perkin Elmer 2100) or, if they were below the
quantification limits of this method, by graphite furnace
spectrophotometry (Perkin Elmer AAnalyst 600).
Quality control of the digestion process was provided by
parallel analyses (1 for every 10 samples) of certified ref-
erence materials (CRMs) within all sample batches, and the
possibility of contamination during digestion was con-
trolled by use of analytical blanks (1 every 10 samples).
The CRMs used were PACS-1 (marine sediment) for soil,
GBW07604 (poplar leaves) for mosses and oak leaves,
BCR no. 186 (pig kidney) and NIST 1577b (bovine liver)
for mammals, and CRM 278R (mussel tissue) for slugs.
Data Analysis
Bivariate Spearman’s rank correlation was used to test the
relationships between trophic compartments (soil-vegeta-
tion, soil-wood mice, soil-shrews, soil-slug, vegetation-
wood mice, vegetation-shrews, vegetation-slug, and wood
mice-shrews). The 0.05 significance level was adjusted
with a Dunn-Sidak correction based on the number of
correlations generated to control for type I errors associated
with multiple comparisons (Sokal and Rohlf 1995).
To test for significant differences between the two
sampled soil sections, the Wilcoxon test was used. Data
analyses were carried out with the statistical package SPSS
13.0.
Results
Limits of Quantification Limits (LOQ) and Reference
Materials
The LOQ (lg g-1) for each essential element and the
recoveries for the different certified materials are reported
in Table 1. Most of the recoveries obtained were satisfac-
tory. Recovery of Fe (range, 112%–142 %) was the worse
of all of the studied elements.
Descriptive Statistics
The concentrations of Cu, Fe, Mn, and Zn in all of the
compartments studied are reported in Tables 2a and 2b. The
order of abundance of the elements in soil was Fe [Mn [ Zn [ Cu. Although the concentrations were similar,
there were significant differences (p \ 0.05) between the
upper and the lower soil layers for Cu (Z = -0.499;
p = 0.012) and Fe (Z = -3.309; p = 0.001). The highest
mean concentrations of these two metals were observed in
the upper soil layer (15–30 cm) (Table 2a). The highest
concentrations of Cu and Zn in soil corresponded to one of
the SSs located at the restored mine dump (SS1), the highest
concentrations of Fe were found at the SS located in the
ultrabasic area (SS3), and the highest concentrations of Mn
at the latter site and at SS16.
The metal concentrations in oak leaves were, usually
(except for Cu–although not always—and Mn), below
those observed in terrestrial mosses and the pattern of
bioaccumulation followed the order Mn [ Fe [ Zn [ Cu
(Table 2a). For mosses, the mean concentrations decreased
as follows: Fe [ Mn [ Zn [ Cu.
The concentrations of metals in slug samples are sum-
marized in Table 2b; the pattern of bioaccumulation
followed the order Mn [ Zn [ Cu [ Fe.
The concentrations of metals in wood mouse and yel-
low-necked mouse were almost identical in all organs
and SSs (Tables 2a and 2b). The order of abundance of the
studied elements in the rodent species was Fe [ Zn [Cu [ Mn. The concentrations of all metals, except Zn,
were generally higher in shrews than in rodents. In general
terms the order of abundance of Zn, Fe, and Mn in the
different tissues of all the species of small mammals was
Table 1 Quantification limit and recoveries for Cu, Fe, Mn, and Zn
in the studied matrices
Matrix Quantification limit (lg g-1)
Cu Fe Mn Zn
Soil 0.075 4.127 0.100 0.636
Moss and oak leaves 0.052 2.225 0.100 0.081
Mammals, organs 0.124 0.946 1.976a 0.689
Slugs 0.027 0.974 0.538 0.396
Recovery (%)
PACS-1 (marine sediment) 98 NCV 78 101
GBW07604 (poplar leaves) 95 112 103 109
BCR no. 186 (pig kidney) 102 133 85 100
NIST 1577b (bovine liver) 114 142 86 100
CRM 278R (mussel tissue) 86 NVC 93 93
Note. NCV, certified value not availablea ng g–1
694 Arch Environ Contam Toxicol (2008) 55:691–700
123
Page 5
Ta
ble
2a
Co
nce
ntr
atio
ns
(lg
g-
1d
.w.)
of
Cu
,F
e,M
n,
and
Zn
inso
il(l
evel
s:0
–1
5an
d1
5–
30
cm),
mo
sses
,o
akle
aves
,an
dw
oo
dm
ice
atth
est
ud
ied
sam
pli
ng
stat
ion
s(S
Ss)
Met
alL
evel
/
org
an
SS
1S
S2
SS
3S
S4
SS
5S
S6
SS
7S
S8
SS
9S
S1
0S
S1
1S
S1
2S
S1
3S
S1
4S
S1
5S
S1
6
So
ilC
u0
–1
58
6.8
42
.42
7.9
33
.01
6.8
2.3
4a
12
.11
0.2
42
.82
8.3
15
.81
7.1
29
.31
2.2
7.8
01
2.2
15
–3
08
9.9
66
.63
1.6
35
.71
6.4
2.7
4a
13
.11
8.3
49
.03
4.9
18
.81
7.1
26
.91
4.4
8.0
81
1.0
Fe
0–
15
60
,00
03
6,6
00
76
,70
05
6,0
00
25
,00
07
,17
01
8,0
00
21
,00
03
8,0
00
42
,80
03
0,3
00
24
,00
03
2,9
00
20
,00
01
3,8
00
28
,30
0
15
–3
06
4,0
00
60
,00
08
6,0
00
61
,20
02
6,0
00
11
,90
01
7,0
00
24
,20
03
9,4
00
42
,80
03
4,0
00
25
,30
03
5,3
00
23
,20
01
4,6
00
32
,00
0
Mn
0–
15
42
02
50
1,4
80
18
82
04
69
.73
98
13
01
80
25
02
20
49
53
94
17
42
25
1,6
60
15
–3
03
84
49
01
,49
02
18
2,0
40
79
.83
98
15
01
74
32
12
73
40
84
28
24
43
60
1,6
00
Zn
0–
15
25
07
6.8
44
.45
1.5
44
.89
.79
a6
0.0
38
.46
7.7
74
.74
0.8
11
52
06
38
.43
8.8
80
.0
15
–3
02
28
12
73
5.8
55
.54
2.8
8.6
8a
59
.64
0.4
88
.08
3.8
43
.41
21
71
.03
9.4
50
.57
1.0
Mo
ssC
u1
0.9
9.4
78
.70
11
.06
.66
8.2
84
.18
5.2
54
.58
6.9
77
.17
4.2
86
.26
4.7
47
.00
6.4
6
Fe
23
81
,27
06
77
47
05
55
34
02
56
58
63
00
55
61
86
26
67
40
10
68
3.8
23
6
Mn
14
21
98
10
12
32
22
22
80
14
21
45
13
31
76
43
02
22
19
02
72
52
53
74
Zn
45
.58
5.8
65
.07
9.8
42
.05
6.0
23
.42
9.9
32
.35
4.5
59
.04
4.8
28
.93
8.0
37
.84
6.5
Oak
leav
esC
un
.d.
n.d
.n
.d.
12
.87
.90
9.4
94
.60
6.3
65
.45
6.4
64
.50
4.0
84
.34
5.5
54
.10
4.3
4
Fe
n.d
.n
.d.
n.d
.1
66
88
.01
17
58
.67
1.0
78
.87
9.8
79
.81
08
56
.66
8.7
46
.51
20
Mn
n.d
.n
.d.
n.d
.3
29
38
65
75
47
03
40
29
92
59
76
75
20
44
48
48
98
01
,10
0
Zn
n.d
.n
.d.
n.d
.2
3.6
18
.22
2.8
14
.81
6.9
14
.71
5.6
17
.01
7.0
15
.01
9.4
15
.81
9.8
Wo
od
mic
e
n2
54
54
01
76
04
11
16
21
63
33
26
41
33
26
21
Cu
L2
5.6
24
.21
9.6
18
.82
2.2
24
.01
9.0
15
.71
5.6
20
.81
8.2
18
.72
0.9
17
.01
9.6
20
.2
K3
3.0
30
.92
7.8
26
.63
0.6
37
.32
0.8
23
.01
9.8
21
.22
2.4
20
.62
0.2
21
.22
1.0
23
.1
B2
1.2
20
.22
0.0
21
.22
4.8
19
.91
9.3
21
.21
9.0
21
.61
9.7
18
.32
0.4
20
.01
5.0
n.d
.
Fe
L9
10
88
07
00
79
08
38
1,1
00
90
91
,10
08
78
75
09
29
86
87
97
76
77
70
76
7
K5
96
47
45
50
57
65
95
60
61
05
05
85
42
88
40
58
54
50
43
06
16
44
85
20
B2
18
21
22
12
22
21
95
23
82
06
23
62
16
22
01
99
19
81
76
16
81
90
16
4
Mn
L8
.80
5.7
54
.10
4.1
44
.78
5.3
53
.26
3.8
93
.53
3.8
03
.93
5.0
54
.64
4.3
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Arch Environ Contam Toxicol (2008) 55:691–700 695
123
Page 6
liver [ kidney [ brain, whereas the tissue distribution of
Cu was kidney [ liver [ brain. Only Mn and Zn in mouse
tissues (with one exception at SS10) followed the same
pattern of bioaccumulation among the tissues at all the SSs
studied; in the case of shrews, this was observed only for
Fe and Mn (with one exception at SS16). The accumulation
of Cu in brain and liver of shrews followed a less clear
pattern (Table 2b).
Comparison of Metal Contents in Natural
and Anthropogenic Ecosystems
The samples from the SSs located in the mine zones
(SS1 and SS2) and in the ultrabasic area (SS3) contained
higher concentrations of all the metals than samples from
natural ecosystems. For this, the 95% quantiles were cal-
culated for each metal and type of sample from the natural
ecosystems (SS4 to SS16); whether or not the values cor-
responding to the other three sites (SS1, SS2, and SS3)
belong to these distributions (p B 0.05) is indicated in
Table 2a. In general, for the soil, at SS1 and SS2 the values
exceed the 95% quantile for Cu, Fe, and Zn, whereas at SS3
the values exceeded this limit for Fe and Mn. For the
moss, all of the values at SS2, except for Mn, exceeded the
corresponding quantiles. In A. sylvaticus, for all metals in
liver, except Fe, the values at SS1 and SS2 exceed the cor-
responding quantiles; the same was true for Zn at SS1 and
SS2 and for Mn in kidneys at SS2. Finally, at SS3 there was
Table 2b Concentrations (lg g -1 d.w.) of Cu, Fe, Mn, and Zn in yellow-necked mice, shrews, and slugs at the studied sampling stations (SSs)
Metal Organ SS1 SS2 SS3 SS4 SS5 SS6 SS7 SS8 SS9 SS10 SS11 SS12 SS13 SS14 SS15 SS16
Yellow-necked
mice
n 17 7 19
Cu L n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 19.2 n.d. n.d. 18.6 n.d. 19.7
K n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 21.2 n.d. n.d. 22.0 n.d. 21.6
B n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 8.80 n.d. n.d. 15.5 n.d. 12.5
Fe L n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 900 n.d. n.d. 630 n.d. 696
K n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 498 n.d. n.d. 737 n.d. 510
B n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 180 n.d. n.d. 154 n.d. 175
Mn L n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 4.86 n.d. n.d. 5.35 n.d. 4.86
K n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 3.82 n.d. n.d. 4.64 n.d. 4.74
B n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 1.37 n.d. n.d. 1.48 n.d. 0.12a
Zn L n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 144 n.d. n.d. 174 n.d. 152
K n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 114 n.d. n.d. 136 n.d. 125
B n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 75.0 n.d. n.d. 79.1 n.d. 93.0
Shrews n 12 6 5 7 15 2 1 14 2 7
Cu L n.d. n.d. n.d. 37.3 36.8 31.3 n.d. n.d. n.d. 30.3 29.0 23.8 46.6 29.6 32.6 28.3
K n.d. n.d. n.d. 118 53.0 53.5 n.d. n.d. n.d. 32.3 35.3 51.0 87.8 30.3 57.6 32.3
B n.d. n.d. n.d. 53.5 64.6 48.4 n.d. n.d. n.d. 20.8 19.2 36.0 64.6 18.6 41.8 20.4
Fe L n.d. n.d. n.d. 1,224 2,200 1,010 n.d. n.d. n.d. 1,545 990 510 1,222 1,000 1,212 1,171
K n.d. n.d. n.d. 520 797 515 n.d. n.d. n.d. 747 710 279 242 616 398 1,444
B n.d. n.d. n.d. 289 464 214 n.d. n.d. n.d. 203 350 146 133 208 210 284
Mn L n.d. n.d. n.d. 12.8 10.4 12.0 n.d. n.d. n.d. 15.0 26.3 23.6 21.2 23.6 20.0 49.5
K n.d. n.d. n.d. 12.0 8.34 7.00 n.d. n.d. n.d. 7.81 8.88 14.7 5.28* 7.80 7.87 19.1
B n.d. n.d. n.d. 1.95 2.60 1.61 n.d. n.d. n.d. 1.74 2.56 3.15 2.45 2.02 1.92 2.29
Zn L n.d. n.d. n.d. 112 224 192 n.d. n.d. n.d. 88.9 85.0 71.7 82.8 89.9 76.7 84.0
K n.d. n.d. n.d. 144 212 252 n.d. n.d. n.d. 89.0 96.9 58.6 83.8 88.9 69.7 80.0
B n.d. n.d. n.d. 66.6 66.0 64.6 n.d. n.d. n.d. 65.6 64.2 72.7 35.9 94.0 47.4 85.8
Slugs n 22 11 43 49 41 37 7 52 16
Cu n.d. n.d. n.d. n.d. n.d. n.d. 67.4 69.7 99.9 88.9 101 68.6 79.7 90.0 84.8 n.d.
Fe n.d. n.d. n.d. n.d. n.d. n.d. 242 84.8 43.4 70.0 51.0 70.0 48.5 52.5 65.0 n.d.
Mn n.d. n.d. n.d. n.d. n.d. n.d. 636 5,918 797 1,212 3,737 1,343 1,171 3,748 2,346 n.d.
Zn n.d. n.d. n.d. n.d. n.d. n.d. 410 448 234 394 343 212 192 280 192 n.d.
Note. L, liver; K, pair of kidneys; B, brain; n.d., not determined; n: number of subsamples included in the analyzed composite samplesa Concentrations below the quantification limit
696 Arch Environ Contam Toxicol (2008) 55:691–700
123
Page 7
no enrichment of any of the metals in any of the visceral
organs.
Relationships Between Trophic Compartments
No significant correlations have been found between the
different types of samples for the studied elements.
Bioaccumulation Pattern in the Different Trophic
Compartments
As regards the metal bioaccumulation in the different
organisms studied at the woodland sites (SS4–SS16)
(Fig. 2), there was a common pattern at most of the sites.
For Cu, the pattern was slugs [ shrews [ mice [soil [ moss * oak leaves; for Fe, soil [ shrews [ mice [moss [ oak leaves [ slugs; for Mn, slugs [ oak lea-
ves [ soil * moss [ shrews [ mice; and, finally, for Zn,
slugs [ mice [ shrews [ soil [ mosses [ oak leaves.
At the woodland sites (SS4–SS16) the concentrations of
the metals were higher in consumers than in producers
(with the exception of Mn) and higher in secondary con-
sumers than in primary consumers (except for Zn). The
highest concentrations of Cu, Mn, and Zn were in the
detritivorous compartment; the highest levels of Fe were in
the soil compartment (Fig. 2). At the remainder of the SSs
(SS1–SS3) the same trends were also observed, with the
exception of the relationship between Fe levels in con-
sumers and those in producers at SS2 (Tables 2a and 2b).
Discussion
A key step in this type of study is selection of the species. In
the present study, the species selected were the dominant
species within each trophic level of the ecosystem. It can be
difficult to find species that are included in a single trophic
level. Thus, in the present study, mice were included as
primary consumers, although they also sometimes eat
invertebrates, and slugs were considered detritivores, but
are also grazers. However, these species are frequently used
as biomonitors and there is abundant information about
Liver : 32.623.8-46.6
Kidney : 55.130.3-118
Brain : 38.718.6-64.6
SECONDARY CONSUMERSShrew
Liver : 19.315.6-24.0
Kidney : 23.619.8-37.3
Brain : 20.115.0-24.8
PRIMARY CONSUMERSWood mouse
PRODUCERS
SOIL
Liver : 19.218.6-19.7
Kidney : 21.521.2-22.0
Brain : 12.28.8-15.5
Yellow-necked mouse
6.364.18-11.0
Moss
6.154.08-12.8
Oak leaves
19.82.34-42.8
0-15 cm
22.02.74-49.0
15-30 cm
DETRITIVOROUS
83.367.4-101
Slug
CuLiver : 1210
510-2200Kidney : 626
242-1444Brain : 250
133-464
SECONDARY CONSUMERSShrew
Liver : 868750-1100
Kidney : 595428-1050
Brain : 202164-238
PRIMARY CONSUMERSWood mouse
PRODUCERS
SOIL
Liver : 747630-900
Kidney : 580498-737
Brain : 170154-180
Yellow-necked mouse
36083.8-740
Moss
87.346.5-166
Oak leaves
274007170-56000
0-15 cm
2960011900-61200
15-30 cm
DETRITIVOROUS
80.743.4-242
Slug
Fe
Liver : 21.510.4-49.5
Kidney : 10.47.00-19.1
Brain : 2.231.61-3.15
SECONDARY CONSUMERSShrew
Liver : 4.403.26-6.20
Kidney : 3.842.40-4.78
Brain : 1.280.96-1.46
PRIMARY CONSUMERSWood mouse
PRODUCERS
SOIL
Liver : 5.004.86-5.35
Kidney : 4.403.82-4.74
Brain : 1.000.12-1.48
Yellow-necked mouse
258133-525
Moss
570259-1110
Oak leaves
35369.7-1660
0-15 cm
37379.8-1600
15-30 cm
DETRITIVOROUS
2320636-5918
Slug
MnLiver : 111
71.7-224Kidney : 117
58.6-252Brain : 66.5
35.9-94.0
SECONDARY CONSUMERSShrew
Liver : 155124-218
Kidney : 12895.6-162
Brain : 73.064.5-91.1
PRIMARY CONSUMERSWood mouse
PRODUCERS
SOIL
Liver : 156144-174
Kidney : 125114-136
Brain : 82.875.0-93.0
Yellow-necked mouse
44.023.4-79.8
Moss
17.714.7-23.6
Oak leaves
71.09.79-206
0-15 cm
63.68.68-121
15-30 cm
DETRITIVOROUS
300192-448
Slug
Zn
Fig. 2 Diagrams showing the
concentrations (lg g-1) in the
different trophic compartments
located in the mature unpolluted
woodlands of Quercus robursampled and the possible
transfer of the essential metals
studied. White triangles indicate
atmospheric inputs and black
triangles indicate edaphic inputs
of metals
Arch Environ Contam Toxicol (2008) 55:691–700 697
123
Page 8
them in the literature. Having opted to use these species,
study of the direct trophic relationships between them, as
well as the possibility of calculating bioaccumulation and
biomagnification coefficients, was no longer possible. In
this case there were only direct trophic relationships
between the mice and the oak (mice eat acorns) and
between slugs and the different species (principally oak).
However, the selection of these species also guaranteed
similar periods of accumulation, given their longevity
(approximately 8–12 months). No top predators were
included because in this type of ecosystem the best (most
abundant and representative) species would be the tawny
owl (Strix aluco), and as this is a protected species, it cannot
be captured and killed.
The comparison between natural and anthropogenic/
ultrabasic ecosystems as regards the atmospheric (repre-
sented by the mosses) and edaphic inputs (represented by
the soil) revealed similar patterns, which suggests that the
moss reflects the deposition of edaphic particles in sus-
pension. As regards the viscera of A. sylvaticus, in the liver
samples the concentrations of Cu and Zn were highest at
the SS in the mine zones. The absence of enrichment of Fe
in the viscera, despite the high concentrations in the soil,
suggests effective homeostatic regulation of this metal. In
contrast, the high concentrations of Cu in liver and Zn in
liver and kidney in the mine zone SS may be related to the
high inputs of these metals in the soil. Finally, the
enrichment of Mn in the viscera cannot be explained by
either edaphic or atmospheric inputs.
The present results demonstrate the lack of close rela-
tionships among the trophic compartments studied. In this
type of study, one of the correlations to which most
attention has been given is that existing between the organs
of small mammals and the total soil concentrations. As in
the present study, the absence of any relationship is com-
mon, appearing, for example, in Milton et al. (2003) for Cu
and in Torres and Johnson (2001) for Zn. However, other
authors who used a soluble fraction observed significant
correlations (p \ 0.05) between the concentration of Cu in
this fraction and that in kidney of A. flavicollis (Folkeson
et al. 1990). This correlation may be attributed to the direct
ingestion of soil particles and transfer through the food web
(Torres and Johnson 2001). As indicated in the previous
paragraph, the higher concentrations of Cu and Zn in the
soil (at a depth of 15–30 cm) coincide with the higher
concentrations of these elements in the liver of A. sylvaticus.
This, combined with the absence of correlations between
soil and viscera, suggests that there may be a threshold
above which the wood mouse’s capacity to regulate these
metals is lost. On the other hand, no relationship between
the total content of metals in soil and that in plant samples
was obtained in the present study. As Torres and Johnson
(2001) pointed out, this may reveal a low level of transfer
between these two compartments. The relationships
between the total contents in soil and those in vegetation
have previously been described for Zn (see, e.g., Milton
and Johnson 2002), although some authors did not observe
any correlations between the concentrations of Cu in these
compartments (Torres and Johnson 2001). As described
above, the use of the soluble fraction allowed identification
of significant correlations for some elements, such as Cu,
Fe, and Mn, for some of the species studied (Folkeson et al.
1990). Other studies have shown correlations between
organs of small mammals and potentially ingested vege-
tation: Folkeson et al. (1990) reported a correlation
between Cu content in beech (Fagus sylvaticus) nuts and
hepatic Cu in A. flavicollis; and Torres and Johnson (2001),
between the concentrations of Cu in seeds of the bullrush
(Scirpus robustus) and that in the liver of Mus musculus.
There was a generally low degree of overlap among the
concentrations of metals in the different trophic compart-
ments, demonstrating a pattern of biomagnification (Fig. 2).
This pattern was particularly evident for Cu, in contrast with
the findings of others author in relation to the contents of
primary consumers and producers and the soil. Milton et al.
(2002) reported lower concentrations of Cu in A. sylvaticus
than in soil and vegetation, and Torres and Johnson (2001)
reported lower concentrations of Cu in liver of M. musculus
than in Scirpus robustus and soil. Nevertheless, as regards
the relationship between primary and secondary consumers,
the present results are consistent with those reported by
Hunter et al. (1987a) and Talmage and Walton (1991). In
both of these studies, higher concentrations of Cu were
observed in shrews (S. araneus) than in mice (A. sylvaticus)
and field voles (Microtus agrestis). The lower concentration
of the metal in A. sylvaticus may be explained by the fact
that the main source of food in this species is seeds (Watts
1968; Eldridge 1969; Butet 1986; Castien 1994), even
though it is an omnivore (Hunter et al. 1987a), and
according to Talmage and Walton (1991), the transfer of Cu
from plant to seeds is low. In contrast, shrews are carnivores
(Hunter et al. 1987a; Castien 1994), in which there is no
decrease in the translocation rate. Furthermore, accumula-
tion of Cu in mammals may be affected by dietary levels of
proteins (Torres and Johnson 2001), and the differential
ingestion of proteins by the two species may also contribute
to the differences found.
In the present study, these elements diverged from the
pattern observed for Cu: in the case of Fe, the transfer-
ence between soil and primary producers was practically
nil, and for Mn, the concentration in the oak leaves was
higher than in the soil, but the transfer of this element
from producers to primary consumers was also practically
nil. Little attention has been focused on these elements in
previous studies, and so it is not possible to make
comparisons.
698 Arch Environ Contam Toxicol (2008) 55:691–700
123
Page 9
Unlike for Cu, with Zn, there were no significant dif-
ferences in the concentrations in primary and secondary
consumers. This finding contrasts with previous reports in
the literature, in which the concentrations of Zn in small
rodents were lower than in shrews, which are placed at a
higher level in the trophic web. Thus, Roberts and
Johnson (1978), Scharenberg and Ebeling (1996), and
Mertens et al. (2001) observed higher levels of Zn in
S. araneus than in A. sylvaticus-A. flavicollis. As regards
the other compartments, various authors (Johnson et al.
1978; Scharenberg and Ebeling 1996; Mertens et al. 2001;
Milton and Johnson 2002; Blackbern, 2003) have reported
higher concentrations of Zn in vegetation samples than in
soil samples, and Mertens et al. (2001) reported that the
concentrations in both of the latter were higher than in
small mammals.
Conclusions
In conclusion, we observed a lack of correlations among
trophic compartments, possibly caused by the effective
regulation of metals by organisms and/or spatial variation
in availability of metals from soil or food. However, in
general terms the overlap between the ranges of concen-
trations of successive trophic levels was very low, which
demonstrates that biomagnification occurs along the tro-
phic chain. Finally, there were no differences between the
unpolluted woodlands and the polluted sites in terms of
these patterns, although there were enrichments in the
concentrations of Cu, Mn, and Zn in the mice viscera,
which, except for Mn, were related to the higher edaphic
concentrations.
Acknowledgments The present study was funded by the Xunta de
Galicia (Project ‘‘Banco de Especımenes Ambientales de Galicia. 3a
Fase’’) and the Ministerio de Educacion y Ciencia (Programa Nac-
ional FPU). Thanks are due to Luıs Brandon, Montserrat Bravo,
Paloma Choucino, Sandra Gonzalez, Mercedes Noya, and Alfonso
Punal for carrying out the chemical analyses.
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