Full text of DOI:10.1002/etc.5620210111

Environmental Toxicology and Chemistry, Vol. 21, No. 1, pp. 76–80, 2002
2002 SETAC
Printed in the USA
730-7268/02 $9.00 .00
᭧
0
ϩ
THE IMPORTANCE OF THE GUT AND ITS CONTENTS IN PREY AS A SOURCE OF
CADMIUM TO PREDATORS
L
EE A. WALKER, LUCINDA J. BAILEY, and RICHARD F. S HORE
*
NERC Centre for Ecology and Hydrology, Monks Wood, Abbots Ripton, Huntingdon, Cambridgeshire PE28 2LS, United Kingdom
(
Received 29 March 2001; Accepted 15 May 2001)
Abstract—Many mammalian and avian predators consume the whole carcass of their small mammal prey. Thus, the contaminant
load of the gut and its contents may be of toxicological significance, but pollutant loads in the gut of prey species are often not
measured and their role in food-chain transfer of contaminants is largely unquantified. We investigated the importance of the gut
and its contents in prey as a source of cadmium (Cd) to predators by measuring the Cd concentrations in the guts (including
contents), in various body tissues, and in the intact bodies of wood mice (Apodemus sylvaticus). The mice had been fed for up to
3
65 d on either control, a medium-Cd (MCd) diet, or a high-Cd (HCd) diet that had nominal Cd concentrations of 0, 8, and 40 g/
g wet weight, respectively. In wood mice fed contaminated diets, Cd was progressively bioaccumulated in all the body tissues that
were analyzed. The gut (and contents) and the liver and kidneys (the critical organs) contained most of the accumulated Cd and
were the only significant contributors to the total body burden (TBB). The contribution of the gut (and contents) to the TBB was
greater in mice fed MCd diet than in those given HCd feed but declined with age (equivalent to exposure duration) in both groups
as Cd in the critical organs increasingly became the most important source of TBB Cd. However, the gut and its contents contributed
between 50 and 100% of the Cd TBB in mice fed for up to six months on MCd diet; this was the diet that most closely mimicked
the estimated average Cd intake of wood mice on contaminated sites. The results of this study highlight the importance of including
measures of Cd load in the gut when modeling food-chain transfer from small mammals to their predators.
Keywords—Cadmium
Total body burden
Food-chain transfer models
Wood mice
Gut contents
INTRODUCTION
The aim of the present study was to investigate the im-
portance of the gut and its contents as a source of Cd to
predators. The specific objectives were to quantify the con-
tribution of the gut and gut contents to the cadmium TBB of
a small mammal and to measure how this varied with dietary
Cd intake and duration of exposure. Such information is need-
ed to determine the importance of including gut content Cd
concentrations in food-chain transfer models and in associated
risk assessments of contaminated sites. The study was carried
out under controlled laboratory conditions rather than by ex-
tensive sampling in the wild so that duration and magnitude
of exposure could be measured accurately; both factors are
extremely difficult, and often impossible, to quantify in free-
living animals. The wood mouse (Apodemus sylvaticus) was
used as a model species because it is widely distributed
throughout Europe, occurs on most polluted habitats, and is
an important prey item for many mammalian and avian pred-
ators, such as small mustelids and owls [13].
Cadmium is a toxic, nonessential metal that can occur in
elevated environmental concentrations as a result of anthro-
pogenic activities such as the smelting of metals (particularly
lead and zinc), mining, disposal of sewage sludge, and appli-
cation of fertilizers [1,2]. It is readily transferred through the
food chain and accumulated by small mammals [3–7]. The
critical organs (the organs that first attain their critical con-
centration of the metal, above which organ toxicity occurs;
[
8]) for Cd are the kidneys and liver. Long-term exposure of
vertebrates to Cd primarily results in nephrotoxicity, although
effects may also be seen in the liver and reproductive, immune,
skeletal, and cardiovascular systems [8–10]. Impacts at the
population level have been described for at least one wild
vertebrate species [11].
Numerous studies have shown that, on Cd-contaminated
sites, approximately 80% of the Cd total body burden of small
mammals is located in their liver and kidneys [1 for reviews,
7
,9]. However, the contents of the gastrointestinal tract are
MATERIALS AND METHODS
often excluded when small mammal carcasses are analyzed
and are not always included in the measure of total body
burden (TBB) or carcass concentration [3,7]. Many mamma-
lian and avian predators consume the whole of their small
mammal prey and, although some raptors egest the indigestible
parts as pellets, these tend to be composed of fur and bone
and not soft tissues. Thus, the Cd load of the gut contents, if
substantial, may well be of toxicological significance to pred-
ators of small mammals, but the lack of data makes it difficult
to incorporate this component into food-chain models and it
has been ignored [12].
The diet given to wood mice was contaminated with Cd by
incorporating cadmium chloride into a standard laboratory pel-
leted diet (Rat and Mouse Diet 1E (P), Special Diet Services,
Witham, Essex, UK). We used three diets that varied in their
Cd content, i.e., a high-Cd (HCd) diet that nominally contained
4
0
␮
g/g wet weight Cd, a medium-Cd (MCd) diet with a
nominal Cd concentration of 8 g/g (wet wt), and a control
␮
diet that was uncontaminated. The diets were analyzed to con-
firm their Cd content.
Wood mice were maintained exclusively on their experi-
mental diets from weaning. The dams of these animals had
also been maintained on the experimental diets throughout
2
*
To whom correspondence may be addressed (rfs@ceh.ac.uk).
their pregnancies. Mice were housed in plastic cages (950 cm
7
6

The gut and its contents as a source of cadmium to predators
Environ. Toxicol. Chem. 21, 2002
77
Table 1. Dry weight (dry wt) cadmium concentration in the control, medium-cadmium (MCd), and high-cadmium (HCd) diets and in the guts
and their contents) of wood mice ( 21 d old) fed these diets; the estimated daily cadmium intakes of mice on each diet are also given and are
estimated from mean daily dry food intake (181.4 g/kg BW/d; L.A. Walker, unpublished data) and the cadmium concentration (dry wt) for each
(
Ͼ
diet; SD
ϭ
standard deviation;
n
ϭ
number of replicates; BW
ϭ
body weight; variance (see text for details) can be calculated as the square of
the SD
Cadmium concentration (
␮
g/g)
Gut and contents
Estimated Cd intake
(mg/kg BW/d)
Diet
SD
Diet
Mean
n
Mean
SD
n
Mean
SD
n
Control
MCd
HCd
Ͻ
0.79
6.89
—
2.70
9.96
5
10
11
Ͻ
0.87
5.74
—
3.91
15.7
44
32
43
Ͻ
0.14
1.25
6.35
—
0.491
1.81
5
10
11
35.0
31.1
ϫ
20 cm high) with stainless steel wire tops and kept pre-
bridgeshire, UK) using deuterium background correction, an
air-acetylene flame, and acid matched standards. Three repeat
measurements were made for each sample. The limit of de-
tection (LD) for the Cd concentration in the analyzed digest
dominantly in same-sex sibling groups after being separated
from the parent pair at 40 d old. The mice were maintained
constantly on a 15-h light:9-h dark photoperiod at 18 to 20ЊC,
and food and distilled water were provided ad libitum. Indi-
vidual male and female mice were killed by cervical dislo-
cation at ages that ranged from 7 to 365 d old. The wet weight
of the intact carcass was recorded at death and the body was
was 0.06
in the tissues (using the mean sample dry wt for each tissue)
of 1.6 g/g (kidneys), 1.2 g/g (liver), 0.87 g/g (guts), 1.6
g/g (testes), and 1.2 g/g (excised carcass). Blanks and sam-
␮g/ml. This corresponded to a mean dry weight LD
␮
␮
␮
␮
␮
stored at
Ϫ
20
Њ
C until it was dissected. On dissection, the liver,
ples of a certified reference material (reference material 186,
Community Bureau of Reference, Commission of the Euro-
pean Communities, Brussels, Belgium) were run at the same
time as unknowns. Cd concentrations in blanks were below
kidneys, gastrointestinal tract (including its contents), and tes-
tes (male mice) were removed, weighed, and oven dried at
8
0
Њ
C for 24 h, by which time the tissues had reached constant
weight. The remainder of the body (defined here as the excised
carcass) was oven dried at 80 C for 48 h before being snap
the LD. The mean (
of Cd from the certified reference material was 81
35). The Cd concentrations of the diets were determined by
inductively coupled plasma mass spectrometry (ICP-MS) with
an associated LD in the sample of 0.79 g/g (dry wt).
Cadmium concentrations are expressed on a dry weight
basis ( g Cd/g tissue) and are not recovery corrected. Cal-
Ϯ
standard error [SE]) percentage recovery
Њ
Ϯ
1.6% (
n
frozen in liquid nitrogen and then homogenized with a pestle
and mortar. The homogenate was mixed thoroughly and a 2-
g subsample was taken and dried at 80
All diet and tissue samples were solubilized in cold (Aristar
grade) nitric acid (Merck, Poole, Dorset, UK) for at least 24
ϭ
Њ
C for 24 h.
␮
␮
h. The samples were further solubilized by heating to 90
at which point 0.5 ml of hydrogen peroxide was added to aid
the oxidation of lipids in the samples. The samples were then
Њ
C,
culated Cd intakes are expressed on a mg Cd/kg body weight
(BW)/d basis. The significance of the relationships between
the age of the wood mice and the Cd residues in the various
body organs was determined by Spearman rank correlation
analysis.
heated to 120ЊC and digestion was allowed to proceed to com-
pletion, which was when the tubes had stopped fuming and
the digests were straw colored. The digests were made up to
a fixed volume with deionized water. The acid content of the
final digest was always 10%, and typically, the final volume
for kidney digests was 5 ml and between 10 and 20 ml for
digests of the other tissues and diet.
RESULTS
The measured concentrations of Cd in the MCd and HCd
diets were close to the nominal concentrations (Table 1); the
Cd concentration in the control diet was below the limit of
detection. The differences in Cd concentration between the
diets were reflected by the gut Cd concentrations measured in
With the exception of the diets, digests were analyzed by
microinjection (170
␮l aliquots) flame atomic absorption spec-
trophotometry (Solar 969, ThermoUnicam, Cambridge, Cam-
weaned (Ͼ21 d old) mice. Cadmium concentrations in the guts
of all mice fed the control diet were below the limit of de-
tection. The fivefold difference in Cd between the MCd and
HCd diets was mirrored by a 5.4-fold difference in gut Cd
concentrations in mice fed those diets (Table 1). However,
there was also a significant positive correlation between the
age of the animal and the concentration of Cd in the gut and
its contents in mice fed both MCd and HCd diets (Fig. 1),
indicating that there was an accumulation of Cd by the gut in
mice fed contaminated diets.
There was almost no detectable accumulation of Cd in the
body tissues by the 44 mice fed the control diet. Cadmium
concentrations were below the limit of detection in the testes,
critical organs (liver and kidneys combined), and excised car-
cass in all mice given the control diet except for two that had
trace critical organ Cd concentrations (0.32 and 0.54 ␮g/g dry
wt). Wood mice fed the MCd and HCd diets did accumulate
Cd concentrations, increasing progressively with age. This was
Fig. 1. The dry weight concentration of cadmium in the gut and their
contents of female ( ) and male ( ) wood mice fed medium-Cd
MCd) and high-Cd (HCd) diets. Note that the -axis scales differ in
the two graphs. Concentrations in all mice fed control diet were not
detected. Spearman rank correlation coefficient and statistical signif-
icance are shown on the graphs.
⅜
ⅷ
(
y

7
8
Environ. Toxicol. Chem. 21, 2002
L.A. Walker et al.
Fig. 3. Proportion of the total body burden (TBB) of cadmium present
in the gut (including contents) and critical organs in female (
male ( ) wood mice fed medium-Cd (MCd) and high-Cd (HCd) diets.
Only weaned individuals ( 21 d old) were analyzed. Spearman rank
⅜) and
ⅷ
Ͼ
correlation coefficient and statistical significance are shown on the
graphs.
transformation, t36
ϭ 0.565, p Ͼ 0.05). This was presumably
because variation in the Cd content of the HCd diet was small
compared with the high Cd TBB of mice fed this diet.
The contribution that the gut and its contents and the critical
organs made to the TBB was examined in mice fed the con-
taminated diets. The proportion of the TBB that was present
in the gut and its contents declined significantly with age
Fig. 2. The dry weight (dry wt) concentration of Cd in the critical
organs (liver and kidneys combined) and body with and without the
gut and its contents of female (⅜) and male (ⅷ) wood mice fed
medium-Cd (MCd) and high-Cd (HCd) diets. Concentrations for mice
fed the control diet are not shown (see text for explanation). Spearman
rank correlation coefficient and statistical significance are shown on
the graphs.
(
equivalent to duration of exposure) in mice fed either the
MCd or HCd diet (Fig. 3). However, the gut and its contents
made up at least 50% of the TBB in all but four of the animals
fed the MCd diet and almost 100% of the TBB in the youngest
animals. Overall, it was the major component of the TBB in
mice aged up to approximately six months old. In contrast,
the contribution of the gut to the TBB was lower in mice fed
the HCd diet, reflecting the greater rate of accumulation of Cd
in the critical organs by these animals (Fig. 2). Despite this,
the gut and its contents contributed more than 50% of the TBB
in 12 of the 20 animals that were six months old or less and
up to 77% of the TBB in the youngest animals (Fig. 3). It was
only in mice more than nine months old that the gut and its
contents generally contained less than 25% of the TBB.
In mice fed both the MCd and HCd diets, the proportion
of the TBB in the critical organs was positively and signifi-
cantly correlated with age (Fig. 3), these organs becoming
increasingly important as the major repository for Cd as ex-
posure continued. This relationship was the mirror image of
that for the gut and the gut contents, reflecting that the gut
and its contents and the critical organs were the only significant
contributors to the Cd TBB.
most marked in the critical organs, and there was a positive
correlation between critical organ Cd concentration and age
in mice fed the MCd and HCd diets (Fig. 2). Cadmium was
also accumulated in the testes by male mice fed the most
contaminated diet. Of the 26 males fed the HCd diet, 21 con-
tained detectable levels of Cd in the testes (data not shown)
and there was a positive correlation with the age of the animal
(rs ϭ 0.760, p Ͻ 0.0001, degrees of freedom [df] ϭ 24). None
of the male mice fed the MCd diet accumulated detectable
levels of Cd in the testes. Accumulation of Cd elsewhere in
the body was negligible. Cadmium concentrations in the ex-
cised carcass were below the limit of detection in all animals
fed either of the contaminated diets except for one mouse fed
the HCd diet that contained 3.25 ␮g/g dry weight.
The Cd concentration in the intact body of each mouse was
calculated by summing the total amount of Cd detected in the
various components of the body and dividing this value by
the summed dry weights of the tissues. In mice fed the con-
taminated diet, the Cd concentration in the intact body in-
creased significantly with age (Fig. 2). The relationship was
relatively weak for mice fed the MCd diet, and this appeared
to be largely due to variation between animals in gut Cd con-
centration. When the gut and its contents were excluded from
the analysis, the relationship between age and body Cd content
DISCUSSION
This study highlighted and quantified the major contribu-
tion that the gut and its contents can make to the Cd TBB in
small mammals. Although the study was laboratory based, the
exposure of the captive wood mice mimicked as closely as
possible that experienced by free-living animals. Small mam-
mals on contaminated and uncontaminated sites have Cd in-
takes of between 0.1 and 25 mg/kg BW/d, although average
(
Fig. 2) was significantly improved (Fisher’s
t24 3.06, 0.01). This was not the case for mice fed the
HCd diet, for which exclusion of the gut contents from the
analysis (Fig. 2) made no significant improvement (Fisher’s
Z transformation,
ϭ
p Ͻ
Z

The gut and its contents as a source of cadmium to predators
Environ. Toxicol. Chem. 21, 2002
79
intakes by wood mice do not usually exceed 2 mg/kg BW/d,
and wood mice accumulate liver and kidney Cd residues of
TBB was trivial. Cadmium was also assimilated in the testes
by wood mice fed the HCd diet, but the amount was relatively
up to 20 and 40
␮
g/g dry weight, respectively (see [9,14,15]
small (
Ͻ2.2% of that accumulated in the critical organs), and
for data reviews). The experimental dietary Cd concentrations
in the present study resulted in Cd intakes (Table 1) and liver
and kidney residues (Fig. 2) in captive wood mice that spanned
and were representative of those in free-living mice. Although
it might have been expected that the exposure of wood mice
in the laboratory would have been unrealistically uniform com-
pared with that of free-living mice that can take food items
that vary in Cd content, there was no evidence that this was
the case. The variance of the measured Cd intake by mice
given the MCd diet (0.24 mg/kg BW/d; Table 1) was actually
greater than that of wood mice from a metal refinery site (0.019
its contribution to the TBB was also minor. Overall, it was
only the critical organs and the gut (including contents) that
contributed significantly to the Cd TBB.
Although differences in the consistency of Cd intake be-
tween captive and free-living animals may not be particularly
marked, variation in gut Cd load between individual animals
may still be relatively high; the gut Cd concentration of mice
fed the MCd diet ranged from 0 to 16.5 ␮g/g. The consequence
of this is that the relative importance of the gut as a source
of Cd to a predator will vary from one prey item to the next
and will be determined by what the prey consumed just before
it was captured. This was apparent in the present study from
the way gut Cd load affected the significance of the relationship
between body Cd concentration and age in mice fed the MCd
diet (Fig. 2). Variation in gut Cd burdens may be more pro-
nounced in free-living rodents in habitats where contamination
is patchy.
Another factor affecting the significance of the gut as a
source of Cd to predators is the age of the prey animal. In the
present study, age was essentially equivalent to the duration
of exposure because weaned mice fed immediately and always
on a contaminated diet. This is also likely to be true in free-
living animals inhabiting sites where the contaminated area is
large, relative to home range size, and so animals are always
exposed to contaminated forage. On such sites, the magnitude
of the Cd TBB and the proportion of the TBB that comes from
the gut will effectively be age dependent, with TBB increasing
and the proportion of TBB contributed by the gut decreasing
with age (see Figs. 2 and 3). This will have consequences for
predators that preferentially take prey of a certain age class or
body size (body wt being a rough corollary to age [19]). Tawny
owls (Strix aluco) prefer heavier bank voles (Clethrionomys
glareolus) [20], while juvenile voles appear to be more vul-
mg/kg BW/d; variance ratio [VR] test, F(31,11)
.01) and did not differ from that (0.24 mg/kg BW/d) of field
voles (Microtus agrestis) from the same site (VR test, F(11,31)
1.44, 0.05; data taken from [5]). Similarly, the variance
in the measured gut Cd concentration of wood mice fed the
MCd diet (15.3 g/g; Table 1) was greater than or not different
from the corresponding values for wood mice (5.06
ϭ 12.6, p Ͻ
0
ϭ
p Ͼ
␮
␮
␮
g/g; VR
g/g; VR
test, F(31,13)
test, F(31,17)
ϭ
ϭ
3.01,
1.32,
p
p
Ͻ
Ͼ
0.05) and field voles (11.5
0.05) from a tailings dam [16]. Even
the variance in the average Cd intakes of wood mice from 10
different polluted and uncontaminated areas (variance of 0.3
mg/kg BW/d; data from [9]) was similar to that of the wood
mice fed the MCd diet (Table 1). Given these similarities in
Cd intake and tissue residues and the exposure consistency
between the wood mice in the laboratory and free-living an-
imals, it is considered that the results of the present study are
both relevant and applicable to mice on Cd-polluted sites.
This study has shown that the contribution of the gut (and
contents) to the Cd TBB of wood mice varies with the amount
of Cd in the diet. It was originally anticipated that, the higher
the dietary concentration, the greater would be the contribution
of the gut to the TBB, at least during the initial period of
exposure. In fact, the reverse was true. The gut and its contents
made up a higher proportion of TBB in mice fed the MCd diet
than in those given the HCd diet for the same length of time
nerable than adults to predation by weasels (Mustela nivalis
)
[21]. Assuming that the Cd distribution in wood mice is typical
of rodents generally, the gut (and contents) would constitute
a more important source of Cd to the weasel than the tawny
owl, although overall dietary Cd concentration would be great-
er for the owl. Thus, the importance of the prey gut as a source
of Cd is likely to vary significantly between predators that
have different hunting behaviors. Furthermore, there may also
be temporal variation in both the Cd intakes of predators and
the proportion of intake derived from the prey gut. This is
because small mammal populations are often dominated by
juveniles at the end of the breeding season [13].
One further implication of the results of this study is that
variation in the contribution of the gut to the prey Cd TBB
could affect the bioavailability of Cd to predators. Cadmium
in the prey gut will be at least partly in ionic form in solution
and may be more bioavailable to predators than Cd bound to
metallothionein in organs such as the liver and kidneys. Sub-
sequently, physiological assimilation of Cd by predators may
also be altered. It has been demonstrated that both the total
and the relative amounts of Cd accumulated by the liver and
kidney and the associated toxic effects vary with the form
(metallothionein bound or inorganic) in which Cd is ingested
[22,23]. The predominant form of Cd ingested by predators
and its subsequent impacts on accumulation and possible tox-
icity warrant investigation.
(
Fig. 3). This indicated that the proportion of ingested Cd
assimilated by wood mice was not constant but was actually
greater in animals fed the HCd diet than in those given the
MCd diet. Studies on rat isolated intestine have demonstrated
that fractional absorption of Cd progressively increases with
intestinal Cd concentration [17]. This may well account for
the relatively greater Cd assimilation of mice fed the HCd diet
in the present study. The consequence is that the contribution
of the gut to the TBB is large when dietary Cd concentrations
are low but smaller when Cd intake is high. Thus, on sites
with relatively low levels of contamination, the gut (and con-
tents) will be the only major repository of Cd in mice and the
only significant contributor to the TBB.
The duration of exposure also significantly affected the
extent to which the gut (and contents) contributed to the Cd
TBB. The longer wood mice were given a contaminated diet,
the less important became the contribution of gut Cd to the
TBB, irrespective of whether animals were fed the MCd or
HCd diet. This was primarily the result of progressive bio-
accumulation of Cd in the liver and kidneys. Although Cd was
also bioaccumulated in the gut, presumably due to uptake of
Cd by the intestinal mucosa [18], this contributed little to the
total gut (and contents) Cd concentration (Fig. 1). Thus, its
influence on the proportion that the gut contributed to the Cd
We conclude that, for small-mammal prey species, a large

8
0
Environ. Toxicol. Chem. 21, 2002
L.A. Walker et al.
9
. Shore RF, Douben PET. 1994. The ecotoxicological significance
of cadmium intake and residues in terrestrial small mammals.
Ecotoxicol Environ Saf 29:101–112.
proportion of their Cd TBB can be in the gut and its contents.
Our results highlight that it is important and necessary to in-
corporate data on gut contaminant levels (and how they vary)
into food-chain transfer models in order to enhance our un-
derstanding of the factors that govern pollutant transfer
through food chains. Inclusion of contaminant levels in the
prey gut and their contribution to prey TBB should also im-
prove the accuracy of models used in risk assessment, although
the complex nature of the data may dictate that this is only
possible when using a probabilistic, rather than deterministic,
approach. The results of the present study on Cd are also likely
to be generally applicable to other elements that are poorly
absorbed across the gut and either do not bioaccumulate sig-
nificantly, such as chromium [15], or that bioaccumulate rel-
atively slowly, such as lead and inorganic mercury [24]. It has
been argued that some of these other elements pose a more
significant risk to wildlife than Cd [25]. Better data on the
levels of pollutants in the guts of small mammals and their
relative contribution to the TBB should be gathered for a num-
ber of toxic elements.
1
0. World Health Organization. 1992. Cadmium. Environmental
Health Criteria 134. Geneva, Switzerland.
11. Larison JR, Likens GE, Fitzpatrick JW, Crock JG. 2000. Cadmium
toxicity among wildlife in the Colorado Rocky Mountains. Nature
4
06:181–183.
1
1
2. Jongbloed RH, Traas TP, Luttik R. 1996. A probabilistic model
for deriving soil quality criteria based on secondary poisoning of
top predators. II. Calculations for DDT (DDE) and cadmium.
Ecotoxicol Environ Saf 34:279–306.
3. Flowerdew JR. 1991. The wood mouse. In Corbet G, Harris S,
eds, The Handbook of British Mammals. Blackwell, Oxford, Ox-
fordshire, UK, pp 220–229.
14. Shore RF. 1995. Predicting cadmium, lead and fluoride levels in
small mammals from soil residues and by species-species ex-
trapolation. Environ Pollut 88:333–340.
5. Sheffield SR, Sawicka-Kapusta K, Cohen JB, Rattner BA. 2001.
Rodentia and Lagomorpha. In Shore RF, Rattner BA, eds, The
Ecotoxicology of Wild Mammals. John Wiley, New York, NY,
USA, pp 215–314.
1
1
1
1
6. Cooke JA, Andrews SM, Johnson MS. 1990. Lead, zinc, cadmium
and fluoride in small mammals from contaminated grassland es-
tablished on fluorspar tailings. Water Air Soil Pollut 51:43–54.
7. Goon D, Klaassen CD. 1989. Dosage-dependent absorption of
cadmium in the rat intestine measured in situ. Toxicol Appl Phar-
macol 100:41–50.
8. Bremner I. 1979. Mammal absorption, transport and excretion of
cadmium. In Webb M, ed, The Chemistry, Biochemistry and Bi-
ology of Cadmium. Elsevier/North-Holland Biomedical, Amster-
dam, The Netherlands, pp 175–193.
Acknowledgement—We thank Dan Osborn for comments on a draft
of this manuscript and Peter Rothery for statistical advice.
REFERENCES
1
. Shore RF. 1996. Accumulation of cadmium and lead in woodland
mammals. In Glimmerveen I, ed, Heavy Metals and Trees. In-
stitute of Chartered Foresters, Edinburgh, UK, pp 124–149.
. World Health Organization. 1992. Cadmium—Environmental as-
pects. Environmental Health Criteria 135. Geneva, Switzerland.
. Hunter BA, Johnson MS, Thompson DJ. 1989. Ecotoxicology of
copper and cadmium in a contaminated grassland ecosystem. IV.
1
2
9. Ma WC, Denneman W, Faber J. 1991. Hazardous exposure of
ground-living small mammals to cadmium and lead in contami-
nated terrestrial ecosystems. Arch Environ Contam Toxicol 20:
2
3
2
66–270.
0. Zalewski A. 1996. Choice of age classes of bank voles Cleth-
rionomys glareolus by pine marten Martes martes and tawny owl
Strix aluco in Bialowieza National Park. Acta Oecol 17:233–244.
21. Jedrzejewska B, Jedrzejewski W. 1990. Antipredatory behavior
of bank voles and prey choice of weasels—Enclosure experi-
ments. Ann Zool Fennici 27:321–328.
22. Groten JP, Sinkeldam EJ, Luten JB, van Bladeren PJ. 1990. Com-
parison of the toxicity of inorganic and liver-incorporated cad-
mium: A 4-wk feeding study in rats. Food Chem Toxicol 28:
435–441.
23. Groten JP, Sinkeldam EJ, Luten JB, Van Bladeren PJ. 1991. Cad-
mium accumulation and metallothionein concentrations after 4-
week dietary exposure to cadmium chloride or cadmium-metal-
lothionein in rats. Toxicol Appl Pharmacol 11:504–513.
24. Scheuhammer AM. 1991. Effects of acidification on the avail-
ability of toxic metals and calcium to wild birds and mammals.
Environ Pollut 71:329–375.
Tissue distribution and age accumulation in small mammals.
J
Appl Ecol 26:89–99.
4
5
6
7
8
. Hunter BA, Johnson MS, Thompson DJ. 1987. Ecotoxicology of
copper and cadmium in a contaminated grassland ecosystem. II.
Invertebrates. J Appl Ecol 24:587–599.
. Hunter BA, Johnson MS, Thompson DJ. 1987. Ecotoxicology of
copper and cadmium in a contaminated grassland ecosystem. III.
Small mammals. J Appl Ecol 24:601–614.
. Hunter BA, Johnson MS, Thompson DJ. 1987. Ecotoxicology of
copper and cadmium in a contaminated grassland ecosystem. I.
Soil and vegetation. J Appl Ecol 24:573–586.
. Talmage SS, Walton BT. 1991. Small mammals as monitors of
environmental contaminants. Rev Environ Contam Toxicol 119:
4
7–108.
. Samarawickrama GP. 1979. Biological effects of cadmium in
mammals. In Webb M, ed, The Chemistry, Biochemistry and
Biology of Cadmium. Elsevier/North-Holland Biomedical, Am-
sterdam, The Netherlands, pp 341–421.
25. Beyer WN. 2000. Hazards to wildlife from soil-borne cadmium
reconsidered. J Environ Qual 29:1380–1384.