IE UPTAKE OF CADMIUM AND ... MOLLUSCS AND SHRIMP EXPOSED TO ... CONCENTRATIONS

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N IO Z - R A P P O R T 1990 - 8
IE UPTAKE OF CADMIUM AND COPPER IN BIVALVE
MOLLUSCS AND SHRIMP EXPOSED TO LOW
CONCENTRATIONS
K. Sarala Devi, J.M . Everaarts
Nederlands Instituut voor O nderzoek der Zee
© 1990
This report is not to be cited without the consent of:
Netherlands Institute for Sea Research (NIOZ)
P.O. Box 59, 1790 AB Den Burg,
Texel, The Netherlands
ISSN 0923 - 3210
THE UPTAKE OF CADMIUM AND COPPER IN BIVALVE
MOLLUSCS AND SHRIMP EXPOSED TO LOW
CONCENTRATIONS
K. Sarala Devi*, J.M. Everaarts
NETHERLANDS INSTITUTE FOR SEA RESEARCH
'Present address: National Institute of Oceanography,
Regional Centre, Cochin-682 018,
Kerala, India
NIOZ-RAPPORT 1990 - 8
SUMMARY
The
uptake of
concentrations
mussel),
and in
Cerastoderma edule
under
Each
basis,
groups
of
showed
in
specimens
from the
seawater
accumulated until
cadmium
f ir s t
day*1.
(cockle),
In
Macoma balthica
Cranaon
cranaon
a significant
of
low ambient
edulis
(baltic
(brown
as well
as
different
edulis
after
an i n i t i a l
uptake process,
and ü.
(blue
te llin )
shrimp)
was
level.
until
In
period
juvenile
the
specimens
of
£.
with an uptake-rate
of
0.087
in i t i a l
exposure
end of
cranaon.
pg
by
on a dry
concentration
with an uptake-rate
followed
between control
of
levels.
about
exposure,
taken
4 days,
specimens
of
and
weight
balthica. cadmium was
lag
linearly
period,
difference
concentrations
of
equilibrium
adult
levels
Mvtilus
conditions.
was taken up linearly
order
different
species
whole-body tissue
both metals
adult
at
mollusc
species
experimental
species
exposed
up
the bivalve
the crustacean
studied
In
cadmium and copper
in
of
£.
and
edule
indicating
0.035
pg
a
C d .g '1.
the cadmium uptake was
C d .g '1.d a y'1
an equilibrium
during
the
concentration
le v e l.
Copper accumulated linearly
with
an uptake-rate
concentration
£.
of
cranaon varied
relatively
this
of
high
high
The
for
soft
pg Cu.g * 1.d a y '1, at
tissues
considerably
containing
level of
present
dry wt.
mainly due to
blood pigment haemocyanin,
e d ulis.
copper
concentration
fluctuated
60 p g . g '1
naturally,
M.
a mean ambient
during exposure and
concentration
of
in
around a
Compared to
the presence
these
fluctuation
significant.
concentration
was twice
both
0.14
whole-body
1.8 pg.dm'3. The whole-body copper
copper content
the copper
are not
of
in
as
cadmium
cases
concentration
high
as
and
the
nominally dosed
even lower
tissue
lim it
in
the
experiments
the background concentration
than
acceptable
of
for
metals
(0.2
pg.dm'3)
open ocean waters
the background level
concentration
considered
in
for
were
copper.
below
human consumption.
In
the
1.
INTRODUCTION
In
seawater,
trace
metals
complex-bound to organic
chelated
with
particulate
of
a
colloids,
material
metal
may
uptake by aquatic
accumulate
diffusion
particulates
predominant
suggest
waterphase,
(Engel s i
The
control
of
widely
of
(1975)
shrimps
Most
high
The use of
for
test
of
metal pollution
included
Council
for
studies
studies
levels
concentrations)
(only
for
their
J.P.
Boon and P.A.W.J.
and
to
also
water quality
and
suggestion
have been
for
frequently
Monitoring
uptake
applied
Both,
as
mussels
Programme of
(ICES).
in
generally
the
the field.
On the
to marine organisms,
trace metals
the
basis
Eisle r
to cadmium
than
Bak
for
checking
Director,
National
Institute
She
to carry
during
levels.
copper
at
low
e dulis.
to
The present
than naturally
Mvtilus
the English.
of
this
and
to
Fischer,
L.
the analytical
c r it ic a l
reading
NIO,
of
The f i r s t
Industrial
Oceanography,
Centre of
grateful
out
and
higher
molluscs
Scientific
Regional
is
cadmium
de Wilde for
of
Scientist-in-Charge,
have been confined
concentration
are due to C.V.
Council
Research.
with
support
thank the
fellowship
are
the
tools
ambient
occurring
Cerastoderma
and the brown shrimp Crangon crangon.
Acknowledgement.- Thanks
study-leave.
from
useful
coastal
were more sensitive
slig h tly
by the bivalve
SdillS and Macoma balthica
B.
the water
Crustaceans
the Sea
on cadmium toxicity
with the uptake of
Nolting
in
bioassays
the Joint
crustaceans
in
metals
tissues
Watch.
in
of
to
from the
and teleosts.
concentration
R.F.
in
Exploration
and
evidence
activity
following
the laboratory, and they are
compared to the natural
study deals
mussels
for
and
food
which are the
is
made them
soft
Mussel
animals
of
species
accumulate
attention
the Global
absorption
there
ion
of
may
1983).
has
and their
considerable
toxicological
doses
to
their tissues
research
concluded that
both molluscs
a l.,
form
organisms
uptake mainly occurs
the metal
molluscs
as
are
extensive
(1971)
to
inorganic
and the rate
by
metal
form,
acids,
chemical
ingestion
Cd and Zn,
many
indicators
International
soluble
Sanders s i
and
Aquatic
water
by
ionic
huraic
The exact
a v a ila b ility
and
1985;
such work.
in
For
in
with
organic
toxicity.
example Cu,
in
received
employed
biological
and
of
for
its
the surrounding
proportional
environmental
experiments
it s
to
1972).
many marine organisms
water
Goldberg
also
1977).
for
1981,
a b ilit y
has
but
from
of
and is
preferred
adsorbed
the body surfaces,
in
ai-,
or
dissolved
associated
only determine
(Ph illip s,
surrounding
marine
not
biota
forms
that
occur
(Stumm & B ilin sk i,
metals
across
can
substances,
author
Dona Paula,
Cochin
for
the Netherlands
and
to
the manuscript
wishes
Research,
UNESCO and NUFFIC for
work at
Gerringa
procedures,
Goa and the
granting
the
to
India;
her
award of
Institute
for
a
Sea
2.
MATERIAL AND METHODS
Adult
specimens
of
the
blue mussel
shrimp Cranqon cranaon were collected
respectively,
part
of
from
cockle
in
the
measured
were
for
use
and
were
filtered
experiments
4 days
starvation
werecarried
out
in
water
was
in
by
For
the
system.
and that
content
were
and copper
cm3.min-1
water
of
cadmium and copper
(Table
and
1)
M.
dilution
of
cranaon
balthica
and on consecutive
Pooled
freeze-dried
About
0.1
m
g,
1972).
n itric
2
of
1%
of
shrimps
The
range
animals
acclimatization
(cf.
Tables)
nor
flow-through
temperature of
-
12
contamination
teflon
glass
15°C.
h
light
of
the
materials.
The
of
30
aquaria
°/oo anc^
(60/30/30
from
solution
standard
the
was
of
(Table
days
after
in
seawater
the
and
of
drawn
system was
cm3.rain-1,
so
exchanged at
that
least
the dose was
40
the
once
in
0.2
pg.dm'3,
standard
stock
solution
The exposure time was
24 or
32 days.
4),
in
(10
specimens
20 specimens
were taken before
dosing
weights
stock
with
seawater
0.21
(concentration
3))
wet
m
g
of
were
These
the
1-4).
12 h dark
by dilution
tanks
191).
(Table
as
were
of £.
indicated
in
of
edulis
edule
starting
determined
homogenized dried
the
the
and the
of
organic
(Table
2)
experiment
tables
and
samples were
were carried
extraction
ammonium
of
water
metals
to
out
bombs were kept
10 cm3 in
for
samples,
(DDDC)
isobutyl-ketone
phase
and
(Paus,
suprapur
at
65%
120
°C for
polypropylene
tubes.
each sample.
500 cm3 of
pyrrolidine-dithiocarbonate
After
technique
3 cm3 of
acidified
in water were complexed with
ammonium diethyl-dithiocarbonate
(MIBK).
weighed to the nearest
material
teflon
samples were diluted
The dissolved
sample,
destruction-bomb
added and the
Duplicate destructions
For
the
weight
control
( 1 dm ) and animals
For the decomposition
were used.
intertidal
one tank was used as
solution
was decomposed by an acid
hours.
the
to constant weight.
400
acid
of
continuous
Metal
concentration
factor
the water
and Q .
figures.
sulphate
the experimental
both
Samples
prepared
the metal
The theoretical
for
a
Rectangular
The flow rate
of
24 hours.
50 pg.dm~3,
of
exposition.
doses
cadmium chloride
from
m
,
the baltic
the
the experiment had a s a lin ity
each experiment
used.
metal
of
and/or
loss
applying
cm)
tank for
size
a constant
submerged.
avoided
seawater used
weight
regime of
saturated.
The
from
fed during
weight
a climated room at
continuously
were
3
were observed.
was completely oxygen
the other
specimens
(Tables
and were not
significant
experienced a night-day
circulating
1 and
the westernmost
specimens
by digging
within a narrow
the
no
system in
The animals
in
for
The experiments
seawater
and the brown
of
in
(1-year)
and adult
the bivalves and the
animals
acclimatized
of
the Balgzand
Juvenile
were collected
of
and
and exposure period;
indications
of
edule
edulis
same area.
Length and weight
were selected
Sea.
Cerastoderma
Macoma balthica
mud-flats
were
channels
the Dutch Wadden
edible
t e llin
the
Mvtilus
with beam trawls
(APDC)
extracted
separation
and
water
a mixture
1% diethyl-
into
the complexes
methylin
the
MIBK were destroyed
metals
were
10 cm
teflon
1974).
flow
tubes
Extractions
bench
fitted
contamination
(Merck).
rinsed
by adding
back-extracted
of
for
the
Most materials
with
further
were done
in
concentrated
into
a
in
suprapur
double-distilled
measurement
teflon
a ll
used were teflon
6N HC1 and three
(Kinrade
made or
used
coupled
teflon
5000).
Elmer,
out:
duplicate
model
single
each analysis
The following
experiment/
destruction
pooled dry weight)/
403).
(except
single
each decomposition
duplicate
and
Elmer,
(HGA
model
spectrometer
procedure was
pooled
individuals/
edule because of
low amount of
single
AAS-measurement.
avoid
suprapur
atomizer
(Perkin
replication
sample of
for £.
a laminar
To
water.
Copper was measured with a flame atomic absorption
(Perkin
carried
spectrometer
in
in
Loon,
coated,
times with double-distilled
to an atomic absorption
The
van
were
Cadmium was measured with a heated graphite-furnace
500)
&
container.
chemicals
acid.
and stored
separating-funnels
clean-laboratory
samples,
n it ric
water
analysis
of
Cd
and
Cu/
3.
RESULTS
3.1.
Cadmium uptake
experiments:
The cadmium concentration
f il t e r
during
of
feeder
edulis
the f i r s t
cadmium
4 days
of
in
of
soft
between 0.5
exposure
to a concentration
day and thereafter
the whole-body
varied
(Fig.
1a).
tissues
and 0.6
of
the
pg.g“1 dry wt,
An obvious
accumulation
0.75 p g . g '1 was observed
on the
8th
a plateau was reached.
Cone. Cd (/Jg g-1dry wt.)
1.0 -
Mytilus edulis
0.8
0 .4 -
0 .2 -
1----------1
----------1
----------1
-
Conc. Cd (jug dm-3)
Figure
1.
The total
The uptake of
(pg.g-1 dry weight;
waterphase
a
dose
concentrations
of
respectively.
the common mussel
given
of
0.2
pg.dm-3
and
0.88
15 °C,
concentration
the
with a mean
in
values)
with a control
(•----------• );
pg.dm'3
Mvtilus
in £ whole body soft
Exposure time 32 days,
were measured at
0.59
is
mean and duplicate
(pg.dm-3).
nominal
experiment
cadmium in
cadmium concentration
and £ the
(o— o)
actual
value
the control
edulis.
tissues
and
cadmium
during
the
and exposed,
After
an
experiment,
slig h t ly
(F ig .
The
was
in i t i a l
mean
0.59
aquarium.
the
the
control
comparison
concentration
the
fir s t
water
four
days
progressively
of
the
decreased
1b).
A
in
(ÛCCd
whole-body
during
in
cadmium concentration
pg.dm'3 in
animals
increase
the cadmium levels
soft
cf.
the water
-
0.88
the
soft
CCd(exposed)
tissues
D.W.(control ) ;
between
whole-body
=
in
and
difference
tissues
1)
evidence
for
a relationship
between
the
concentration
at
(Fig.
of
of
2a).
exposed
in
the
cadmium
and
1a)
no
control
and their
D.W.( exposed)
exposure
Also
cadmium in
=
experiment
the
Fig.
(ÛD.W.
a certain
the
in
exposed
Ccd(control ) ; cf.
pooled dry weight
Table
during
pg.dm'3
time
showed no
correlation
whole-body
soft
exists
tissues
and
the mean wet weight.
-
r
0.1
0.1
0.2
0.3
04
0.5
-
- I _____ I_____ I_____ I_____ L_
0.1
0.1
_1_
_l_____ I_____ I_____ I_____ L
0.2
0.3
0 .4
0.5
i
2-
-
0.2
1-
-
0.1
0-
-0
1-
-
Mytilus edulis
-
Cerastoderma edule
2-
AD.W.
0 .2 H
-1
-
0. 2-
-
0 .4 -
2.
whole-body
in
Macoma
0.2
-2
-0
—
1
Crangon crangon
M a co ma balthica
AC r
—I--------------------1-----0.1
(a),
- -
0 .4 -
L
(ÛD.W.
0.1
A D.W.
0-
Figure
- -
The
0 .2
0.3
0.4
0.5
= D.W.(exposed ) juvenile
balthica
-
relationship
(ACCd = CCd(exposed)
cockle
(c)
where o and • refer
to
0.1
0.1
between
-
D.W.(control ))
in
adult
2
0.3
0.4
0.5
the cadmium concentration
in
Cerastoderma edule
and
0.2
Ccd(control ))
two different
—
J
—r~ 1--------1--------—1-----------------r~
1------1--------- 1--------- r
adult
(b),
and
body
mussel
in
dry
in
weight
Mvtilus
edulis
baltic
t e llin
adult
brown shrimp Cranaon crangon
(d),
experiments
10).
(cf.:
p.
9;
Fig.
The results
M-
balthica
linearly,
an
on the uptake of
are
according
uptake rate
+ 0.035
given
* X;
of
r
cadmium by the bivalves
Fig.
to a normal
0.035
N = 7;
in
3.
In £.
f ir s t
order
p < 0.001),
edule
accumulation pattern,
pg Cd.g ' 1.d ay'1 (linear
= 0.968;
£.
and
edule. cadmium was taken up
in
regression:
the
exposed
with
Y = 0.771
specimens.
Cone.Cd (jug-g-1dry wt.)
Cone.Cd (jug g-1 dry wt.)
Exposure time (days)
Figure
edule
3.
(à)
The
concentration
weight;
uptake of
and the baltic
is
given
cadmium in
te llin
mean and duplicate
concentration
Exposure time 32 days,
dose of
pg.dm'3 (•— •)
0.2
0.51
15 °C,
pg.dm'3 in
edible
the
the control
values)
with a control
actual
with a mean value
cadmium
during
and exposed,
cockle
Cerastoderma
(fe). The total
in â and b whole body soft
(pg.dm'3).
measured at
the
Macoma balthica
cadmium
tissues
(p g .g '1 dry
and £ the
waterphase
(o— o)
and a nominal
concentrations
the experiment
respectively.
of
0.45
were
and
However,
it
occurs,
was also
though to
C d .g '1.d a y'1
0.905;
p <
seen that
a lesser
(linear
0.001).
in
untreated animals
extent,
with an uptake
regression:
= 0.649
a
lag-time
concentration
in £1. balthica
increased
dry wt.
exposure
Within
concentration
After
Y
than M.
time £.
The
aquarium varied
exposed
animals
concentrations;
0.45 pg.dm-3
When
that
of
an increase
of
-
decrease
in
balthica.
in
£.
the
In
one
cranaon
with
an
0.077
+ 0.087
fir s t
order
relatively
The
data
difference
the
water
4d),
did
(0.07
of
not
both
show
weight
(cf.
3.2.
In
second
(Fig
(Fig
4,
Mvtilus
5a).
The
slig h t ly
with
soft
2c).
cadmium
the water was
exposed.
it
in
a
in
body
can be concluded
whole-body
significant
dry
(p
soft
< 0.01)
weight).
relationship
the f i r s t
p < 0.05),
pattern
(Fig.
level
in
exposure
In
M-
between these
whole-body of £.
days
of
4a).This
towards
the
(0.86
end of
experiment,
with
cadmium
pg.dm'3
(Fig.
4b).
a very
slight
pg.dm'3)
whole-body
in
(Fig.
cadmium
animals.
correlation
existed
between whole-body
= D.W.( exposed ) -
Moreover,
by a
concentration
(0.46
in
Y =
normal
exposure.
0.17
pg.dm'3)
expressed as ÛCCd = CCd(exposed)
2d).
a
was followed
the water differed
chance
exposure,
regression:
indicating
pg.dm'3) and exposed
no
in
four
pg Cd.g"1.d a y'1 (linear
significant
neither
concentration showed
-
CCd(control)
D.W.(control ) on
the concentration
any relation
to
in
the
the body
4).
experiments:
the
exposure,
copper
the
(Fig.
difference
2b),
tissues
a
exposed and control
Fig.
edulis
during
higher
higher
the
the
(Fig.
) between the mean
tissue
Table
pg.g"1
a
exposed and
cadmium in
= 0.958;
(0.39
any
in
Copper uptake
linearly
only
the
with
such
expressed as ÛD.W.
weight basis
nor
r
experiments,
and body weight,
dry
during
0.087
pg.dm"
both
of
pg.dm'3) and exposed
cadmium concentration,
water
no
concentration
control
concentration,
In
of
(0.69
the
0.45
experiment
concentration
cadmium concentration
of
=
cadmium
2c).
N = 4;
constant
the
pg
r
augmented cadmium concentration
correlated
accumulation
mean
the
the cadmium concentration
linearly
X;
between control
The
(Fig.
uptake rate
*
N = 7;
about
both the
pg.dm'3 in
(whole-body
experiment,
increased
of
slig h tly
animals
cadmium
was
contrary,
parameters was found
only
relatively
the
edule
of
during
Ccd(control ))
body weight
on
the water
and 0.51
the
exposed and control
tissues
X;
days,
to values
concentration
the control
(ACCd = CCd(exposed)
in
considerably
mean
correlating
weight
four
*
0.027
edule accumulated cadmium to
experienced
the
in
+ 0.027
also
of
balthica.
The cadmium concentration
control
of
accumulation
rate
tissue
concentration
with an uptake rate
concentration in
and showed a mean value
maximum and minimum values
of
6.7
of
of
thecontrol
6.4
and 6.0,
of
0.14
copper
pg
specimens
p g.g"1 (S.D.
respectively.
increased
Cu.g " 1.day*1
varied
± 0.3),
with
Conc. Cd (jug g-' dry wt )
Conc.Cd (jug-g-1dry wt.)
0 .8 -
Crangon crangon
0 6
'
O-L
1-1
-1
----------1
---------r~
1 ------------- 1------------- 1-------------- 1-------------- 1------------- 1--------------r ~
I
I
20
24
Conc.Cd (jug d m -3)
Conc.Cd !jug dm-3)
1. 2 -
Sea water
1. 0 -
1------------- 1------------- 1------------- r -
12
16
20
24
12
Figure
4.
The total
dry
The uptake of
weight;
waterphase
a
dose
concentrations
(d)
Exposure
of
0.2
of
(fc)
0.39
of
the brown shrimp Cranaon cranaon.
given
in â and £ whole body
concentration
time 24 days,
pg.dm'3
were measured at
experiment
experiment
is
mean and duplicate
(pg.dm'3).
nominal
f ir s t
cadmium in
cadmium concentration
values)
the
with a mean
and
0.86
and 0.46 pg.dm'3 in
the
(o— o)
actual
value
pg.dm'3
(p g .g '1
and b and £ the
with a control
(•---------•);
15 °C,
0.69
16
Exposure time (days)
Exposure time (days)
during
and
control
the
and
and
cadmium
the
second
exposed,
respectively.
The copper
trend
day
towards
(Fig.
pg.dm*3)
the
5b).
in
experiment
concentration
the
in
Concentrations
exposed than
of
water
showed
8th day and remained almost
1.79
in
were only
control
and 1.50
a
slig h tly
aquaria,
slig h t ly
constant
higher
decreasing
t ill
the
32nd
(about
0.3
with mean values
pg.dm'3, respectively.
during
Cone. Cu (>ugg_ldry wt.)
Exposure time (days)
Figure
5.
The uptake of
The total
(pg.g-1
copper
dry weight;
(pg.dm"3).
a
dose of
were measured at
1.50
Exposure
0.2
15 °C,
an i n i t i a l
copper
followed
cranaon
by
linear
a
in
control
specimens,
the common mussel
the course
at
of
concentration
time 32 days,
the control
day'
increase
during
and exposed,
(Fig.
the
6a).
the copper concentration
only
slig h t ly
lower
the
tissues
and
the
(o— o)
and
concentrations
experiment
of
respectively.
the whole-body concentration
during
again
values)
copper
e d u lis.
soft
with a control
the actual
increase,
decreased
Mvtilus
in a whole body
with a mean value
'f i r s t
in £.
pattern
in
given
pg.dm"3 (•— •)
and 1.79 pg.dm'3 in
After
of
is
mean and duplicate
waterphase
nominal
copper
concentration
ambient
subsequent
7
Remarkably,
the
same
in
the
was observed
concentrations.
days,
The copper
values
levels
during
in
the
water
the experiment of
and exposed groups,
respectively
varied
0.75
(Fig.
considerably,
and 1.05 pg.dm'3 in
with
mean
the control
6b).
Conc.Cu (jug-g-1 dry wt.)
Conc.Cu (jug-dm-®)
1------- 1-------1-------1------- 1------- 1------- 1—
0
Figure
6.
The total
weight;
The uptake of
mean and duplicate
of
15 °C,
body
edulis
copper
is
(Fig.
(•---------•);
the control
was
7a)
of
nor
the brown shrimp Cranaon cranaon.
in à
concentration
whole
values)
with a control
the actual
during
and exposed,
-
in £.
cranaon
(Fig.
(p g .g '1 dry
(o— o)
and a
nominal
copper concentrations
the experiment
of
were
0.75
and
respectively.
Ccd(control))
exposed and control
body
and J* the waterphase
found between the relatively
(ACcd = Ccd(exposed)
weight
in
given
with a mean value
correlation
concentration
in
- 3
pg.dm-
pg.dm"3 in
No
12
16
20
24
Exposure time (doys)
Exposure time 32 days,
0.2
measured at
1.05
8
copper concentration
(pg.dm"3).
dose
4
animals
7b).
augmented copper
and the
(ÛD.W.),
difference
neither
in H-
ADW.
2-
0 .4
1-
0 .2-
0-
0-
ADW.
-1-
Mytilus edulis
2-
L
-
-
0 . 2-
-
0 .4
Crangon crangon
-
L
~l------ 1-----r
-1
3
4
-T-//-T-
5
4
11
A C Cu
Figure
body
7.
The relationship
(ACCd = Ccd(exposed ) -
D.W.(exposed)
-
in
shrimp
adult
4.
brown
Ccd(control ))
Crangon
in
adult
crangon
in whole-
and body dry weight
mussel
Mvtilus
(Ad .W
.
edulis
(a)
=
and
(b).
DISCUSSION
The concentration
considerably
in i t i a l
period of
the
waterphase
are
aquaria,
such as
organisms
the
source for
in
to
obtain
a
susceptible
In
body
low
as
tissues
study,
of
fj.
of
be described
the cadmium
external
concentration
in
wall,
during
circumstances
physiological
concentration
dosed,
low
the
pump,
in
in
the
activity
exposure.
Another
might
be
especially
experiments
the analytical
at
waterphase
biomass during
the present
the concentration
edulis
procedure
concentrations,
and
in
at
in
order
for
metal
is
very
it s
in
the
No
in
the
whole
correlation
relationship
average
levels
a significant
and
same average dose.
concentrations,
cadmium
in
the
content
interspecific
between
there
organism
is
w ill
no
(1986).
difference
the
which
may be related
evidence
reflect
the
environment
specimens
Although uptake rates
with
between
a study by Coleman and coworkers
reveal
concentration
of
showed no significant
cadmium in water.
those data did
the
changing
the
cadmium and copper
the p e rista ltic
Moreover,
cadmium
received
of
especially
accumulation
either
metal
applied
of
However,
to
to the glass
the
the concentration
could
due
of
in
especially
contamination.
the present
soft
in
copper
experiments,
Such fluctuations
mainly
dose.
water,
of
cadmium and
the flow-rate
low pumping rates
in
the various
and the decreasing
the
analysis
to~tal
in
adsorption
variations
irre g u la ritie s
of
exposure.
of
to
Cu
between the copper concentration
D.W.(control ))
varied
in
AC
that
the
environmental
conditions
1976).
(Bryan,
proportion
of
the metal
thereby keep their
the
present
tissue
study,
the
levels,
mussels
al-,
in
1986).
are
are able
intake
contaminated conditions
for
able
to
edulis
ionic
lag
period before accumulation occurs,
complexed
al-
Ritz
(1982)
and
accumulation rate
concentrations,
uptake
that
is
consistent
during
period
the
animals.
in
in
lower
the
edulis
von
accumulation
exposed
Like
failed
in
in
to
matter of
well
in
Westernhagen
shorter
and
al-,
si
period
to concentrations
as
Ritz
exposure
high
higher
pattern
of
(1977)
molecular
values
uptake
during
noticed
marked
and
exposed
mussels,
al-»
si
even
periods
previous
studies
between
(Fowler
was
50-200
as
Also
a
low
relation
uptake
1978,
of
must
1977).
pg.dm'3) and lowest
direct
cadmium
cadmium
observed a significant
experiments,
a
et
i n it i a l
with these data;
also
(2.5
the present
the water
at
(1986)
demonstrate
Coleman
This
between exposed and control
concentrations
the cadmium,
George & Coombs
increase
agree
al-
si
background
shows an
The low and fluctuating
subsequent
concentrations
concentration
to organic
of
exposed to higher
ranges.
of
In
8 days
observed
previously
suggestion
experiments
experimental
also
5% of
1 9 77 ;
concentration were noticed between control
exposure time.
1974;
uptake.
Amiard-Triquet
difference
have
and
present
differences
of
the
at
because
(1986)
higher
and may
levels.
(George & Coombs,
concentration
with
before possible
i n it i a l
at
cadmium in Mlow
about
a
after
weeks
possibly
al-
si
cadmium must be complexed eg.
weight,
the
of
two
cadmium also
can occur
Coleman
even at
normal
(George & Coombs,
exposed to
uptake
excrete
f a ir ly
eliminate
weeks
to
accumulation
During
be
before
at
further
excretion.
the previous
M.
under
concentration
lim it
exposure may be due to
accumulated
Some species
&
1982).
recorded
the
Benayoun,
A linear
on
mussels
pg.dm*3 (George & Coombs,
1 977 ) .
In
Mvtilps
from
Port
elevated cadmium levels
ranging
groups
between
between
cadmium
8.7
10 and 90 m
m (Talbot,
from those data,
of
body size
of
was
0.2
agrees
12.6
concentration
weight basis
(cf.
irrespective
of
of
of
data,
Corio
1985).
The
with a size
Bay,
of
a
value
the different
mean
value
50-60 m
m
,
0.2
pg.dm'3 in
showing
no
2a).
Moreover,
tissues
lower than the
of M-
reported
progressive
increase
at
filtered
size
of
the
calculated
the
(40-50
values
in
of
to
This
between
both on wet-
cadmium
edulis
exposure
seawater.
relationship
cadmium and body weight,
Fig.
a
from
and the body concentration,
levels
in whole-body soft
pg.dm'3 was
contaminated with water with
p g . g '1 at a
cadmium
concentration
in
the
3
.
These data showed no relation between the
the organisms
with the present
measured
0.29
in mussels
pg.dm"
ambient concentration
tissue
Bay,
circulate
and 21.6 p g . g '1 was found for
concentration
seawater
P h illip
which
the
and dry
concentration
m
m
)
exposed to
Talbot
uptake towards
(1985),
the
end of
exposure.
In
the
gradually
exposed
cockle
un til
A
and
occurred
edule
end of
specimens.
between control
cadmium
£.
the
the
the
marked
exposed
according
cadmium
exposure
difference
animals
to
time,
was
a normal
in
concentration
both
in
increased
the control
the concentration
induced.
firs t
order
and
level
Accumulation
proces,
of
both at
mean arabient concentrations
pg.dm'3
(control).
pg.dm'3
results
concentration
towards
in
in
water
concentration
the biological
available
However,
desorption
organisms
of
from
sediments,
eight
days
in
of
in it i a l
caamium in
observed
1979).
significant
In
days
of
balthica
Ray
edule, during
comparison,
different
upon
(cf.
Fig.
of
of
12.5
present
Extensive
organisms
small,
study
both
on
molluscs
control
as
well
to moulting
incidence
of
the
animals.
concentrations
during
high
of
24.4
and
(Cooke
slL
very
low
waterphase
a
the
of H.
McLeese
showed
respectively.
copper
found.
at
&
of
cadmium
However,
even
of
1971).
the
at
The
slig h tly
to
results
large
of
30% loss
of
the
only
(day
A
3)
higher
the
metal
& Benayoun,
animals.
In
the number
observed
(10
in
captivity
the
a low incidence
inluencing
1 and
major
and uptake
of
(Fowler
(1977)
cadmium
of
1976).
amount
cranaon
cadmium
observed
toxicity
eliminated
marine
to
However,
stress
(Ahsanullah,
sign ifica ntly
exposure
toxicity
cannibalism
and
a
is
Dethlefsen
i n it i a l
after
size
cadmium concentration
clams
in
cadmium
level
between the
(Eisler,
the
moulting
concentgraions
a l..
reacted
ambient
was observed by
are
animals
not
an
was
even at
are more sensitive
animals,
bioassay
p g . g '1
from
cadmium.
authors
affect
after
cadmium in
p g . g '1 dry wt.
net-uptake,
with brown shrimp £.
was observed,
experimental
to
of
a
phenomenon may cause up to
experiments
mortality
exposed
during
of
pg.dm'3 no net-uptake was
and teleosts
the
since
in
relationship
show
many
w ill
during
This
1.4
the
2a).
increase
high
in
occurred
increase
the
Fig.
marked
decreased
balthica. evidently
crustaceans
of
experiments
exposed
M-
cadmium
moulting
accumulated
of
as
an
7.3
medium and large
concentrations
studies
encountered by
1974).
of
(Cooke
of
uptake
had not
in
p g . g '1 dry wt.,
did
demonstrated that
are
cadmium
exposure
(cf.
on
cockle,
uptake
showing a cadmium equilibrium
and 8.5
problems
present
t e llin
2b),
14 days,
augmented ambient
leading
took place
An inverse
a much lower concentration
than
of
in
precipitated
actual
been shown that
When exposed to a relatively
21.8,
Thus
to
and ambient cadmium concentration
45 pg.dm'3 for
data
has
such a slight
exposure.
(1984).
levels
days
it
the
to
a concentration
wt.
a
of
reduction
the concentration
at
in
levels
From a study
was achieved by means
concentrations
the baltic
a
lower b io -a v a ila b ility
dry
four
study,
cadmium
way
but
respons
calcium carbonate was
calcium carbonate,
p g . g '1
bioaccumulation
concentration
8
measured,
0.55
ambient
though
No
0.06
in it ia l
exposure.
sediment.
only
resulting
cadmium bound
Unfortunately,
the present
augmented
a
of
in £.
In
the
biogenic
the
0.45
cadmium
The concentration
which the cadmium content
seawater.
value
to
and
the
sediment-bound cadmium to
from the waterphase.
of
due
pattern,
a v a ila b ility
from
of
p g . g '1 in
the end of
considerably
this
the waterphase was not
dry weight
any
edule. whereas
cadmium
occurred
of
difference
concentrations
animals.
towards
(exposed)
cadmium bound to biogenic
to £.
calcium carbonate was
1979).
show
a v a ila b ility
dm*3
0.3
mainly
exposed
not
of
ambient
noticed
was concluded that
readily
pg.
concentration
tissues,
in
did
was
0.51
difference
the
uptake-rate
cadmium
a l ..
a
a
slig h t ly augmented
higher
it
Thus
in
of
in
and
£.
of
minimum
cranaon
20 pg.dm"
).
However,
in
specimens
conditions
after
cadmium had not
exposed
30 days
of
increased
in
of
with respect
of
2.5
the present
to a rapid
of
an
study
accumulation
found.
rise
Also
in
in
another
An increase
s lig h t ly
of
to
a
contrary,
30 days,
times
higher
in
f ir s t
external
sign ifica n tly
during
exposure
an
constant
level.
biological
reaction
characterized
level.
in
Davenport,
starting
and continued
experiment,
w ill
the
no
the f i r s t
long
load was
steep
period
a l-
(1986)
days;
of
is
an
in
of
seawater
shells
for
not
show
any
did
8
16
and
gradually
as a
linear
only
days
a
of
higher
with higher
trace
levels
si.
element
in
lethal
show a physiological
the range of
were
proces
vary
(Amiard-Triquet
(Scott
several
in
copper
slig h tly
the
not
the bioaccumulation
0.5
orders
t ill
the
of
study,
reaction
started
augmented
to
& Mayor,
the present
valve-closing
So accumulation of
in
pg.dm'3,
hours
applied
even
a 330-
copper may be
in
several
to
at
attained
Mussels
the
be reflected
100
essential
1976).
in
e d ulis.
exposure
mussels
exposure
exposure.
the
of
of
to regulate
period of
in £1.
found that
after
These concentrations
at
Thus
mass
than the concentrations
did
copper
concentration
(Bryan,
their
1977).
concentration
of
to organ and decreases
concentrations
even
by
study,
already
even low concentrations
species
individuals
the
four
copper
closing
magnitude higher
copper
concentration
and increasing
marine
Thus,
Due to the low
of whole-body
proces.
visceral
in copper
from organ
to copper
where the
the
Although
mg.dm'3,
order
copper
the f i r s t
processes,
several
1977).
septemspinosa. a
accumulation
The a b ilit y of mussels
contamination
1986).
the total
concentrations
in
increase
copper varies
of
specimens
agree with these data
the present
Cranaon
Amiard-Triquet s i
level
flow
showed a linear
(Dethlefsen,
4a,b)
concentration
applied
pg.dm*3 in
linear
concentration
1972;
Fig.
shrimp species,
augmented copper
body burdens.
10
(cf.
a significant
total
for
pg.dm*3 for
in
constant
1981).
0.3
induces
according
âl-,
the
characterized by an increase
£ i a l-,
(Ray
waterphase,
of
On
the cadmium concentration was found within
exposure
of
under
short-term accumulation
early plateau
ambient cadmium concentrations
term
pg.dm*3
the whole-body concentration
whole-body cadmium concentration
the results
building
1.5
significantly.
exposed to a concentration
increase
to
exposure,
upon
immediately
end
of
ambient
the
copper
concentration.
The
copper
compared
to
concentration
the
experiments.
bivalve
These
65 p g . g '1 dry
wt,
are
bloodpigment
An increase
of
in itiate
copper
in
significant
negligible
Ray
level
and w ill
ai-
to
uptake of
in
animals.
concentration
due
exert
the
very
in
of
yet
it
presence
is
p g . g '1
dry
any physiological
copper
of
the
concentration
in Q .
does
not
whole-body
higher
the
this
effect.
copper
shrimps.
concentration
that
account
wt),
present
the
of
are consistenly
into
high
between 50 and
apperently
remarkable
is
in
varying
Though the copper
taking
60
cranaon
involved
the waterphase
copper.
£.
the body fluid
exposed animals
(around
(1981),
the
However,
not
species
body burdens
haemocyanin
variations,
concentrations
control
molluscs
pg Cu.dm'3 in
showed considerable
whole-body
high baseline
containing
0.3
in
In
than
high
increase
is
a study
of
septemspinosa
exposed to
two
sets
significant
changes
concentration
in
of
During
the
The role
the condition
affecting
1970;
which were subjected to
organisms
M.
of
1972).
a decline
stress
sediments
value,
showed
even
appeared to be high
the present
stre ss',
e dulis.
metals
However,
in
though
(60
have
no
the
pg.dm"
It
of
is
of
)
animals
for
example
excluded
in
Bayne & Thomson,
(1986)
did
not
cadmium in mussels
not very
uptake
the
the
be
al.
rates
influenced
because
not
cadmium;
Coleman s i
stress.
study,
which alters
may
(eg.
accumulation
nutritive
would
significantly,
in
'n u tritive
accumulation
evidence of
nutrition
described
of
Thomson & Bayne,
find
water
and metabolism of
the
i n it i a l
study.
experiments
fed.
contaminated
the
the overlying
compared to the present
were not
highly
from
of
lik e ly
that
metals
relatively
short
in
the
exposure
period.
The data of
between
of
the
the present
whole-body
both cadmium and
balthica
and
experiment
No
£.
copper
apparently did
were
£.
edule. a
the Southern
is
of
the
of
Bight
0.45 pg.dm'3; Kremling
the
lowest
values
The nominal
reflect
twice
for
only
as high
as
species
groups.
importance
of
the
are
in
each
(Duinker
of
now
and only
open ocean
in
10
copper
species
basis.
of
the
of
lower
impact of
"no
environmental
control
than
the
waters
1977).
Sea
It
(0.2
than
(Bruland,
1980)
experiment
levels
open
for
thus
and are only
ocean
waters
copper.
and
tissue
indicate
processes
environment.
in
on aquatic
assessment.
of
the
the
Sublethal
and sensitive
concentrations
in
exposed
showed different
important
-
higher
control
contaminants
effect"
North
These results
from the
increasingly
2b).
to
less
times
physiological
cadmium and copper
evaluation
whole-body
showed marked differences
between
investigated
specific
becoming
is
present
in
1-4).
weight
the coastal
surface water
the
Üthe
the cockle
(Fig.
& Nolting,
augmented contaminant
on a dry weight
a method of
in
from the Central
1988)
dosed
and
determination
can be used as
Sea
the experiments
species
dry
of
Higher
experiment
copper
of
Tables
it s
body weights
than the background level
cadmium
levels
bioaccumulation
studies
used
Moreover,
concentration
North
& Hydes,
slig h t ly
and
specimens
the background concentrations
of
(cf.
pg Cu.dm"3 dosed additional
the values
in
e d u lis.
the course
augmented cadmium
found.
lower
the present
the
as
measured
very
was
to
1.5 pg.dm'3 for
cadmium and even lower
A ll
the
0.3
concentrations
concentration
for
correlation
during
of
tissues
(1-year)
relationship
of
during
the body weight
juvenile
were related
about
same level
affect
fed
a
and the concentration
specimens
being
whole-body
in
of
seawater concentration
background level
of
in
significant
concentration
adult
Not
not
However,
cadmium concentrations
The
in
dry weight
found between the relatively
and copper concentration
2 and 7).
tissues
cranaon.
correlations
(Fig.
study gave no evidence for
soft
l if e
tools
and
contaminants
5.
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M.,
1976.
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M.
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Mobley & N.
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Cambridge University
Mann,
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176-198.
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T.F.
Amiard,
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In:
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Metayer
Mvtilus
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1980.
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7-13.
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Science
Bryan,
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187-196.
Berthet,
Thompson,
Meersunters.
nickel
27:
the mussel
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K.W.,
cadmium and zinc
to the ecotoxicological
keeping Mvtilus
Bruland,
of
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of
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pollutants
biology
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seminar
7-34.
Hickman,
1986.
Mvtilus
cadmium pollution?
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Biol.
92:
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Cooke,
M.,
G.
Nickiess,
a va ila b ility
of
R.E.
Lawn & D.J.
Roberts,
sediment-bound cadmium to
Cerastoderma edule. -
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Environ.
1979.
the
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Biological
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Toxicol.
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386.
Davenport,
J.
1977.
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A study of
the
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in
of
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Mar.
Biol.
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Dethlefsen,
V.,
Ass.
1977.
brown shrimp
Duinker,
J.C.
metals
Bull.
Engel,
Uptake,
Nolting,
retention
1977.
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M.
Brouwer & F.P.
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F.J.
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1971.
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to
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F.J.
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trace
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Comparison of
metal
blue crab and the
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Factors
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Vernberg,
New York:
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1985.
protein
Marine Pollution
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Environmental
Thurberg
Can.
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Thurberg,
metal uptake and toxicity
R.,
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Engel,
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A.
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Calabrese,
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1974.
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International
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George,
S.G.
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Coombs,
1977.
The effects
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Biol.
Goldberg,
39:
J.D.
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E.D.,
1975.
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van Loon,
1974.
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45:
1894-1898.
Kremling,
Co,
K.
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Cu,
Hydes,
Mn and Ni
Continental
McLeese,
D.W.
& S.
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32:
Paus,
Ray,
P.E.,
1972.
1977.
trace
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D.A.,
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B.M.,
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26:
Aust.
K.D.
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in
Cd,
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cadmium CdEDTA
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Toxicol.
biological
materials.
biological
& C.W.
e d u lis. & H.
-
Environm.
J.
Mar.
indicator
Pollut.
1981.
d iffic u lt ie s
larvae.
Mayor,
spéciation.
of
In:
1985.
Bull.
1982.
-
-
13:
to
281-317.
of
copper,
sediments
Bull.
by three
Environ.
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S.H.
The effect
in
143:
679-688.
33:
levels
in
Costlow.
1983.
free
on metallothionein
and
53-54.
of
Trace metals
copper
in
arising
Advances
New York:
Mvtilus
491-506.
(II)
on survival,
the common blue mussel
Jenkins.
Relationship
Res.
222:
the mussel
heavy metal
Effects
rate
1972.
Use of
Sunda & J.D.
sea water:
interpretation
in
study.
Freshwater
1972.
Pergamon.
water and those
organisms
Accumulation
in monitoring
W.G.
in
and heart
Biol.
research.
E llio t,
(Lamarck)
B ilin sk i,
Atomic
in marine and estuarine
A laboratory
Jenkins,
crab
-
315-322.
activity
respiration
V.,
of
Peterson,
Swain & N.G.
ion
Talbot,
& M.R.
planulatus
cupric
W
.
a review.
Toxicol
seawater.
Stumm,
Al,
Is le s.
129-130.
pollution
invertebrates.
edulis
D.M.
-
11:
The use of
metal
McLuser
Contam.
Scott,
Uptake and excretion
cadmium and lead from two contaminated
marine
Sanders,
1984.
dissoved
89-105.
Bomb decomposition
D.J.H.,
zinc,
Ritz,
8:
Newsletter
environments
S.,
Res.
of
around the B ritish
85-92.
monitor
Ray,
Summer distribution
surface waters
by Macoma balthica. -
Absorption
P hillip s,
Shelf
1988.
in
natural
Mvtilus
waters:
from ignorance
on water
on their
pollution
39-52.
between cadmium concentrations
the mussel
Mvtilus
e d u lis.
- Mar.
in
sea
Biol.
85:
51-54.
Thompson,
R.J.
feeding
Ecol. 9:
Westernhagen,
J.
& B.L.
in
1972.
Active
Mvtilus
metabolism associated
edulis
(L.).
-
Mar.
with
J.
Exp.
Biol.
G.
Furstenberg
111-124.
H.
von,
Klinckmann,
experimental
31:
Bayne,
the mussel
471-484.
V.
Dethlefsen,
1978.
marine
H.
Rosenthal,
Fate and effects
ecosystem.
-
of
cadmium in
Helgoländer
Wiss.
&
an
Meeresunters.
Cadmium and copper
and the average
weights
(g)
of
exposure experiment Mvtilus
shell
length
(cm)
the whole- body soft
Length
(cm)
tissues
Exp.
Control
ExDosed
time
Average
Average
(days )
(range )
(range )
5.0
5.0
4.8-5.6
4.6-6.1
Control
Cd çjtDosure
1
2
4
8
16
32
of
5.0
5.1
4.5-6.0
4.4-5.7
4.9
5.2
4.5-5.9
4.5-6.1
5.1
5.2
4.6-5.9
4.6-5.9
5.1
5.2
4.7-5.7
4.5-6.0
5.0
5.1
4.4-5.8
4.4-5.8
4.9
5.0
4.5-5.7
4.5-5.9
4.2
4.7
3.8-4.5
3.8-4.8
(g)
ExDosed
and dry
10 specimens.
Pooled whole-body
wet weight
0
e dulis: the range
and the pooled wet-
soft-tissues
dry weight
Control
(g)
Exposed
experiment
48.1
50. 4
8.28
9.21
42.3
45.8
7.30
8. 49
42.9
53.7
7.41
9.45
44 .0
46.6
7.77
7.58
48. 4
47.3
8.75
8.00
43. 1
46.8
7.13
8.43
49 . 2
47.6
8. 46
8. 23
£ll ejtposure experiment
0
1
2
4
8
16
32
4.8
4.7
4.6-5.0
4.3-5.1
4.8
5.0
4.4-5.3
4.5-5.5
4.9
4.7
4.6-5.3
4.4-5.4
4.9
4.9
4.6-5.2
4.3-5.4
4.9
5.1
4.6-5.1
4.3-5.3
4.6
4.5
4.1-5.4
4.0-5.1
39.0
42.8
4.50
5.04
48.5
41 .6
5. 43
4.44
44.7
47.5
4. 20
5.37
39.4
40.4
4.32
4.31
34.1
33.9
3.86
3.98
34 . 1
35.1
3.58
3.79
37.4
39.3
3.61
3.90
Table
2.
Cadmium exposure
the average
shell
weights
of
(g)
experiment
length
whole-body
Length
Cerastoderma edule: the range
(cm)
(cm)
and the pooled wet-
soft
tissues
of
Exp.
Control
Exposed
time
Average
Average
(range )
(range )
1.6
1.6
1.2-1.9
1.3-2.2
1.6
1.5
1.3-2.0
1.3-2.2
0
1
2
4
8
16
32
1.5
1.5
1.3-1.7
1.3-2.0
1.6
1. 4
1.4-1.9
1.2-1.6
1. 4
1. 4
1.1-1.7
1.1-1.7
1.5
1.5
1.2-1.7
1.2-1.8
1. 4
1. 4
1.2-1.8
1.1-1.8
20 specimens.
Pooled whole-body
wet weight
Control
and
and dry
(g)
ExDosed
soft-tissues
dry weight
Control
(g)
Exposed
7.32
7. 79
0.57
0 .63
6.37
5.72
0.49
0.52
6.84
7. 46
0.45
0.49
6.34
8.11
0.54
0.39
6.48
7.17
0.35
0.34
6.29
5.05
0.34
0. 29
6.21
4.91
0.35
0.21
Table
3.
Cadmium exposure
average
length
experiment Macoma balthica: the range and the
(cm)
whole-body soft
and the pooled wet-
tissues
Length
of
(cm)
Controi
ExDOsed
time
Average
Average
(range)
(range )
0
1
2
4
8
16
32
2.1
2.1
1.9-2.5
1.7-2.3
2.0
2.0
1.6-2.4
1.6-2.4
2.0
2.0
1.6-2.4
1.8-2.2
2.0
2.0
1.7-2.3
1.8-2.2
2.0
1.9
1.6-2.2
1.6-2.3
2.0
2.0
1.7-2.3
1.6-2.5
2.1
1.9
1.7-2.2
1.6-2.2
of
Pooled whole-body soft-tissues
wet weight
Exp.
and dry weights
20 specimens.
Control
(g)
ExDosed
dry weight
Control
(g)
ExDosed
14.5
14.7
2.27
2.22
13.2
12.7
1.86
1.75
14.0
14.2
1.96
2.21
13.4
12.6
1.81
1.64
14.1
14.8
1.85
2.13
13.3
14.0
1.65
2.01
14.3
13.0
1.88
1. 72
Cadmium and copper
wet-
exposure
and dry weights
specimens
exposure
pooled;
I
(g)
of
and I I
experiment
Cranaon cranaon: the
the whole-body tissues
refer
to two separate
of
10
cadmium
experiments.
Pooled whole -body
Exp.
time
wet w
eight
Control
(days)
(g )
dry
w
eight
Ççntççl
Exposed
(g)
ExDosed
Cd exposure experiment
I
/ II
I
/
II
I
/
II
I
/
II
0
25.3
--
21.5
_
_
5.82
/ 2. 23
1
24.3
--
22.0
--
5.25
/ 1.96
4.96
2
24.6
--
23.5
--
5. 43
5.39
4
24.8
--
23.6
--
4.99
2. 02
5.47
8
26.2
--
25.1
--
5.58
/
/
/
2. 14
2. 30
5. 46
/
/
/
/
16
24.2
--
23.9
--
5.97
/ 2. 08
5.32
/ 2. 12
24
19.9
--
12.9
--
4.19
/ 1.89
3.80
/ 1.99
5. 28 / 2.08
Cu exposui:e experiment
0
6.62
6.66
2.45
2. 17
1
6.09
7.32
2.02
2. 23
2
5.85
6.43
2.14
1.99
4
5.87
6.53
1.84
2. 12
8
5. 76
7.08
2.00
2.17
16
6.66
6.35
2 . 40
2.30
24
5.74
4. 48
1.95
1.80
2. 17
2.30
1.93
2.21
NIOZ - RAPPORT 1990 - 8
CONTENTS
1
1. Introduction ................................................................................................................................................
3
2. Materials and methods ..............................................................................................................................
4
3. Results ..........................................
3.1. Cadmium uptake experiments
3.2. Copper uptake experiments .
(0 0)0)
Summary ........................................................................................................................................................
4. Discussion ..................................................................................................................................................
13
5. References ..................................................................................................................................................
18
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