The influence of zinc on the accumulation of cadmium and
copper in the terrestrial isopod Porcellio scaber (Crustacea,
Isopoda)
Vpliv cinka na akumulacijo kadmija in bakra pri kopenskem
enakono`cu Porcellio scaber (Crustacea, Isopoda)
Primo` ZIDAR
Department of Biology, Biotechnical Faculty, University of Ljubljana, Ve~na pot
111, SI-1000 Ljubljana, Slovenia; e-mail: primoz.zidar@bf.uni-lj.si
Abstract. Relative to data derived from single-metal exposure not much is
known about metal kinetics in terrestrial isopods exposed to a mixture of metals. In
the work presented the accumulation pattern of Zn, Cd and Cu were studied in
Porcellio scaber, one of the most investigated isopods. Animals were fed with hazel
leaves dosed with single metals or their binary mixtures. After twenty-one days of
exposure, food consumption and metal accumulation were measured. Results
revealed that the accumulation of Zn is not affected by a decreased food consump-
tion rate or by possible interactions between the mixture constituents. In contrast,
the accumulation of Cd and Cu is significantly reduced when food is also contam-
inated with Zn. The lower accumulation of Cd and Cu can be ascribed to interac-
tions with Zn that affect uptake and/or loss of metals.
Keywords: Isopods, Porcellio scaber, metal mixtures, zinc, copper, cadmium,
food consumption, accumulation
Izvle~ek. Kinetika kovinskih ionov pri kopenskih rakih enakono`cih, ki so
izpostavljeni zmesi kovin je, v nasprotju z izpostavitvijo le eni kovini, malo poz-
nana. V predstavljenem delu smo spremljali akumulacijo cinka, kadmija in bakra
pri kopenskem raku enakono`cu vrste Porcellio scaber. Poskusne `ivali smo hranili
z listi leske, ki smo jim dodali raztopino ene ali pa zmes dveh kovin. Po enaindva-
jsetih dneh izpostavitve smo izmerili koli~ine zau`ite hrane in koli~ino akumuli-
ranih kovinskih ionov. Rezultati so pokazali, da na akumulacijo cinka ne vpliva
upad prehranjevanja kakor tudi ne interakcije med kovinami v zmesi. Nasprotno je
akumulacij kadmija in bakra zna~ilno ni`ja ob so~asni prisotnosti cinka v hrani.
Ni`ja akumulacija kadmija in bakra je posledica njune interakcije s cinkom, kar
vpliva na manj{i privzem ali pa ve~je izlo~anje kadmija in bakra iz telesa.
Klju~ne besede: raki enakono`ci, Porcellio scaber, zmesi kovin, cink, baker,
kadmij, prehranjevanje, akumulacija kovin
ACTA BIOLOGICA SLOVENICA
LJUBLJANA 2005 Vol. 48, [t. 1: 3-12
Sprejeto (accepted): 2005-09-27
stevilka 1_05.qxp  13.12.2005  12:32  Page 3
Introduction
Terrestrial isopods have been successfully adopted as monitor organisms in assessing the
bioavailability of metals (WIESER & AL. 1976, COUGHTREY & AL. 1977, HOPKIN & AL.1986,
DALLINGER & AL. 1992, HOPKIN & AL.1993, CORTET & AL. 1999, PAOLETTI & HASSALL 1999). Many
investigations have proved that they accumulate the highest tissue concentrations of zinc, copper,
lead, and cadmium known for any invertebrate (HOPKIN 1989, CORTET & AL. 1999, HEIKENS & AL.
2001). Their main metal storage organ is the hepatopancreas (WIESER 1961, COUGHTREY & AL. 1980,
HOPKIN & MARTIN 1982) where metals are bound to specific low-molecular-weight peptides
(DONKER & AL 1990, @NIDAR{I~ 2003), or stored as undissolved metal granules (WIESER & KLIMA
1969, PROSI & DALLINGER 1988, HOPKIN 1989). The hepatopancreas of terrestrial isopods consists of
two cell types in which two types of intracellular granules have been observed; B granules in S cells
and C granules in B cells (WIESER & KLIMA 1969, HOPKIN & MARTIN 1982, PROSI & DALLINGER
1988, HOPKIN 1989, HOPKIN & AL. 1989). In isopods collected from contaminated sites both types of
granules contain Zn whereas only B granules contain Cu and Cd (HOPKIN 1989). Zn stored in B cells
can be excreted as these cells show a daily cycle of apocrine secretion whereas Cd and Cu stored in
S cells cannot be excreted because S cells have primarily a storage function and were never observed
to secrete material into the gland lumen (HOPKIN 1990, HAMES & HOPKIN 1991a).
The digestive system is the main route for metal intake in terrestrial isopods. Metal uptake from
food depends on the availability of metals (MARTIN & AL. 1976), the number of micro-organisms in
the gut and food (COUGHTREY & AL. 1980), the nutritional status (FARCAS & AL. 1996), the rate of
food consumption (DROBNE & HOPKIN 1995, BIBI~ & AL. 1997), the temperature (DONKER & AL.
1998), pH inside the gut (HOPKIN 1989), and some other factors.
Relative to data derived from single-metal exposures not much is known about the metal uptake
in terrestrial isopods exposed to mixtures of metals. Interactions between metals in a mixture may
affect the bioavailability of a single metal (VAN GESTEL & HENSBERGEN 1997) and the accumulation
and excretion kinetics may differ when animals are exposed to various metals simultaneously
(WITZEL 2000, ODENDAAL & REINECKE 2004). As isopods in an industrially polluted environment are
usually exposed to several metals at the same time (BEYER & AL. 1984, HOPKIN 1989), some further
investigations with metal mixtures are needed.
In the present work, we studied the accumulation of Zn, Cd and Cu in one of the most investi-
gated isopods, Porcellio scaber, after exposure to single metals or their mixtures. We aimed to show
the importance of such investigations for better understanding of metal accumulation and excretion
kinetics in isopods and for proper interpretation of biomonitoring data.
Materials and methods
Experimental animals and procedure
Specimens of Porcellio scaber raised in the laboratory were used in the experiments. The parental
population was collected in an unpolluted environment in the vicinity of Ljubljana, Slovenia. Juvenile
isopods of 15-25 mg fresh weight were placed in plastic Petri dishes (diameter 9 cm), three animals
per dish (N=36 for each concentration). A filter paper moistened with water was added to each Petri
dish to assure constant humidity. Animals were fed with hazel leaves (Corylus avellana) dosed with
a single metal (Zn, Cd, Cu) or binary mixtures (Zn+Cd, or Zn+Cu) for 21 days. The leaves were col-
lected from an uncontaminated area in autumn. Solutions of ZnCl2 (>98 % pure Merck, Darmstad,
Germany), CuCl2*2H2O (≥99 % pure Merck, Darmstad, Germany) and CdCl2*H2O (>98 % pure
Merck, Darmstad, Germany) were applied to the leaves by spraying. The amount of solution applied
Acta Biologica Slovenica, 48 (1), 2005 4
stevilka 1_05.qxp  13.12.2005  12:32  Page 4
to each leaf was adjusted to give the following nominal concentrations: Zn – 1000 and 3500 mg kg-1
dry weight; Cu – 500 and 2000 mg kg-1 dry weight; Cd – 250 and 500 mg kg-1 dry weight. Actual con-
centrations were analysed and did not differ of those desired by more than 5%. The base concentra-
tions of Zn, Cu and Cd in the control leaves from the collection site were 40 mg Zn kg-1 dry weight,
20 mg Cu kg-1 dry weight and 0.15 mg Cd kg-1 dry weight. Control animals were fed with untreated
food. The experiment was performed in a climate chamber at a relative humidity of 100% and at 16
hours light and 8 hours dark regime. Temperature was kept constant at 21°C (±1°C).
Food consumption was measured as the difference in the weight of leaves at the beginning and
at the end of the experiment. Food consumption rates (CR) were calculated as the absolute consump-
tion of food per week divided by the dry weight of the animals.
Metals concentration analyses
After exposure to the metal treated food, animals were food deprived for 24 hours to empty their
guts. Then they were lyophilised, weighed and completely digested in a nitric/ perchloric acid mix-
ture (7:1). After evaporation of the acid, the residue was taken up in 0.1% HNO3. Total Zn, Cu and
Cd concentrations in whole animals were determined by flame atomic absorption spectrometry
(Perkin Elmer AAnalyst 100). As certified reference material a Dogfish Liver (DOLT-2, National
Research Council Canada) was used. The leaves were analysed for metals in the same way.
Statistical analyses of data
Data on metal accumulation and food consumption rates were analysed using two-way ANOVA
with the factors Zn concentration in food (3 levels), Cd concentration in food (3 levels), Cu concen-
tration in food (3 levels), and the food consumption rate as the covariate (the criteria for significance:
p<0.05). For each metal concentration or combination used accumulation of a single metal was cor-
related with food consumption rate by using Pearson’s correlation coefficient (the criteria for signif-
icance: p<0.05). For all statistical analyses the SPSS 12.0 for Windows software was used.
Results
Accumulation of cadmium and zinc
The concentration of Cd in control animals and animals fed with only Zn-dosed food did not
exceed 2 mg kg-1 dry body weight. Animals exposed to food contaminated with 250 and 500 mg Cd
kg-1 dry food weight accumulated up to 400 mg Cd kg-1 dry body weight (Fig. 1). Cadmium accumu-
Primo` Zidar: The influence of zinc on the accumulation... 5
0
50
100
150
200
250
300
350
400
450
500
0 Cd 250 Cd 500 Cd
C
d
(m
g/
kg
dw
)
0 Zn
1000 Zn
3500 Zn
Figure 1: Concentration of Cd in Porcellio scaber after three weeks exposure to food contaminated
with Zn or Cd or their mixture (AVR±SE).
stevilka 1_05.qxp  13.12.2005  12:32  Page 5
lation from food was significantly lower where Cd in food was combined with Zn (Tab. 1). Cadmium
accumulation was in general correlated with the food consumption rate which decreased with the
increased concentration of both Cd and Zn in food (Fig. 3). No correlation between accumulated Cd
and accumulated Zn was found.
Accumulation of Zn (Fig. 2) was not dependent on food consumption rate (Tab. 1 and Fig. 3). In contrast
to Cd, the accumulation of Zn from food even slightly increased when offered in a mixture with Cd (Fig. 2).
Accumulation of copper and zinc
The concentration of Cu in control animals and animals fed with Zn-dosed food was around 200
mg kg-1 dry body weight (Fig. 4). The copper concentration in Cu treated animals increased with
increasing Cu concentration in food. Animals exposed to food contaminated with 3500 mg Zn kg-1
food in a mixture with 500 or 2000 mg Cu kg-1 food accumulated significantly less Cu compared to
animals fed with only Cu-contaminated food. 1000 mg Zn kg-1 food did not affect the accumulation
Acta Biologica Slovenica, 48 (1), 2005 6
Table 1: ANOVA (p values) for Zn, Cd and Cu accumulation in Porcellio scaber after 21 days of exposure
to food dosed with a single metal (Zn, Cd, or Cu) or binary metal mixtures (Zn+Cd or Zn+Cu). 
0
100
200
300
400
500
600
700
800
0 Zn 1000 Zn 3500 Zn
Zn
(m
g/
kg
dw
)
0 Cd
250 Cd
500 Cd
Figure 2: Concentration of Zn in Porcellio scaber after three weeks exposure to food contaminated with
Zn, Cd, or their mixture (AVR±SE).
stevilka 1_05.qxp  13.12.2005  12:32  Page 6
of Cu. In general, the food consumption rate had no significant effect on the accumulation of Cu,
although the consumption rate decreased with increasing concentration of Zn and Cu in food (Fig.
6, Tab. 1). On the other hand, in animals exposed to 500 mg Cu kg-1 + 3500 mg Zn kg-1 food, Cu
accumulation significantly correlated with food consumption rate.
The accumulation of Zn was affected neither by the Cu concentration in food nor by the food
consumption rate (Tab. 1) and increased with increasing concentration of Zn in food (Fig. 5).
Primo` Zidar: The influence of zinc on the accumulation...  7
0
1
2
3
4
5
6
0 Cd 250 Cd 500 Cd
C
R
(m
g/
m
g 
dw
)
0 Zn
1000 Zn
3500 Zn
Figure 3: Food consumption rate (CR) in Porcellio scaber after three weeks exposure to food contaminat-
ed with Zn, Cd, or their mixture (AVR±SE).
0
200
400
600
800
1000
1200
0 Cu 500 Cu 2000 Cu
C
u
(m
g/
kg
dw
)
0 Zn
1000 Zn
3500 Zn
Figure 4: Concentration of Cu in Porcellio scaber after three weeks exposure to food contaminated with
Zn, Cu, or their mixture (AVR±SE).
0
100
200
300
400
500
600
700
800
0 Zn 1000 Zn 3500 Zn
Zn
(m
g/
kg
dw
)
0 Cu
500 Cu
2000 Cu
Figure 5: Concentration of Zn in Porcellio scaber after three weeks exposure to food contaminated with
Zn, Cu, or their mixture (AVR±SE).
stevilka 1_05.qxp  13.12.2005  12:32  Page 7
Discussion
Our results demonstrated lower accumulation of Cd and Cu in Porcellio scaber after exposure to
food dosed with Zn+Cd or Zn+Cu mixtures compared to single metal exposure. In contrast, the accu-
mulation of Zn was nearly unaffected by the presence of Cd or Cu. The changed accumulation pat-
tern for Cd and Cu can be attributed to a changed food consumption rate or to interactions between
the mixture constituents.
Metal intake may be avoided by regulation of the food consumption rate (DROBNE & HOPKIN
1995, ZIDAR & AL. 2003b) or by food selection (KASCHL & AL. 2002, ZIDAR & AL. 2003a, 2004,
2005). The two selected concentrations of Zn, Cd, and Cu used in our experiment were previously
determined as the concentrations with no major impact on food consumption rate and as concentra-
tions that decrease the food consumption rate in short term exposure to a single metal (ZIDAR 2000).
In contrast to our previous finding, 1000 mg Zn /kg and 500 mg Cu /kg were recognised as concen-
trations that already affect food consumption rate. In a mixture, all metal concentrations decreased
food consumption. At all concentrations used the food consumption rate was correlated with accu-
mulation of Cd, but not with Cu or Zn accumulation, although the latter had the strongest effect on
food consumption rate. This proved that Cd accumulation could be reduced by the regulation of food
consumption rate, as found in our previous studies (KASCHL & AL. 2002, ZIDAR & AL. 2003ab, ZIDAR
& AL. 2005).
Beside food consumption rate, chemical and physiological interactions between food con-
stituents might also affect metal bioavailability. It is known that Cd has a higher affinity for chloride
ions than Zn (reviewed in RAINBOW 1997) which affects the uptake of Cd from the substrate in
collembolans (VAN GESTEL & HENSBERGEN 1997). In isopods Cd complexation with chloride most
probably does not affect the uptake of Cd. HAMES & HOPKIN (1991b) found an even higher assimi-
lation rate for Cd compared to Zn when both metals were offered in a mixture as chloride salts (100
mg Zn/ kg + 100 mg Cd/ kg dry food weight). In Porcellio laevis exposed to food contaminated with
a Zn and Cd sulphate mixture, lower accumulation of Cd was observed (ODENDAAL & REINECKE
2004). Copper is not known to complex with chloride but it has stronger affinity for organic ligands
than Zn (HERTZ & AL. 1990). POSTHUMA & AL. (1997) reported that Cu reduced the sorption of Zn to
soil whereas Cu sorption was inert toward Zn addition. In contrast to our findings, Cu also stimulates
the uptake of Zn in Enchytraeus crypticus (POSTHUMA & AL.1997).
Elevated concentrations of Zn might either reduce Cd and Cu uptake or increase their loss from
storage sites in P. scaber. The only significant route by which metals can be assimilated or excreted
Acta Biologica Slovenica, 48 (1), 2005 8
0
1
2
3
4
5
6
0 Cu 500 Cu 2000 Cu
C
R
(m
g/
m
g 
dw
)
0 Zn
1000 Zn
3500 Zn
Figure 6: Food consumption rate (CR) in Porcellio scaber after three weeks exposure to food contaminat-
ed with Zn, Cu, or their mixture (AVR±SE).
stevilka 1_05.qxp  13.12.2005  12:32  Page 8
in terrestrial isopods is via the digestive system: via the cells of the hepatopancreas and papilate
region of the gut (HOPKIN & MARTIN 1984, HAMES & HOPKIN 1989). There are two potential major
mechanisms for the uptake of dissolved trace metals in crustaceans; binding to metal-specific mem-
brane carriers, or entry via routes used in the uptake of major ions like Ca (RAINBOW 1997). The later
route is known for Cd (WRIGHT 1977), whereas Zn uptake does not appear to follow any route for
major ion uptake (RAINBOW & DALLINGER 1993). Evidence from studies on invertebrates suggests
that assimilation of Zn into cells is regulated metabolically whereas Cu transport is strictly passive,
dependent solely on the extracellular-intracellular gradient (summarised in HOPKIN 1993). Once in
the cell, Cu and Cd are bound to a sulphur-containing ligand whereas Zn is bound to phosphate
(HOPKIN 1993). DONKER (1992) found that the more Zn is stored in the hepatopancreas of P. scaber
the lower is the proportion of Cd accumulated in this organ, while the concentration of Cd in the
remainder of the body increased. DONKER (1992) assumed a limited storage capacity for metals in
the hepatopancreas. The study of WITZEL (2000) revealed a significant increase in uptake and excre-
tion of Cd and Zn when exposed to Zn and Cd simultaneously. WITZEL (2000) assumed that com-
bined contamination with Cd and Zn inhibits the complete translocation of the assimilated metals
into the hepatopancreas. Probably a fraction of Zn and/or Cd remains in the haemolymph or in other
tissues, which can be excreted more easily (WITZEL 2000). This means that Zn might compete with
Cu or Cd for metal-specific membrane carriers or for binding sites in metal binding proteins when
entering the cell.
Conclusions
In Porcellio scaber the accumulation of Zn is not affected by decreased food consumption rate
or by possible interactions between mixture constituents. In contrast, the accumulation of Cd and Cu
is significantly reduced when food is also contaminated with Zn. The lower accumulation of Cd and
Cu can be ascribed to metal interactions that affect uptake and/or loss of metals and which should be
taken into account in biomonitoring data evaluation.
Acknowledgements
This work was financially supported by the Slovenian Ministry of Education, Science and Sport
(projects No. Z1-3189 and PO-0525).
Povzetek
Kopenski raki enakono`ci so pomembni pokazatelji obremenjenosti okolja s kovinami, saj
kovine v telesu kopi~ijo. Kovine sprejemajo prete`no s hrano, skozi prebavilo, skladi{~ijo pa zlasti
v celicah prebavnih `lez, vezane na nizko molekularne beljakovine ali pa v netopnih granulah.
Koli~ina privzetih kovin je odvisna od koli~ine zau`ite hrane, koli~ine mikroorganizmov v hrani in
prebavilu, dostopnosti kovin v okolju, pH prebavnih sokov, temperature v okolju in drugih
dejavnikov. Interakcije med sestavinami hrane in kovinami lahko vplivajo na dostopnost, akumu-
lacijo in izlo~anje kovin. Podatkov o medsebojnem vplivu razli~nih kovin v zmesi na privzem
posamezne kovine je malo. Kopenski enakono`ci so v industrijsko onesna`enem okolju obi~ajno
izpostavljeni visokim koncentracijam ve~ kovin hkrati, zato so raziskave o medsebojnem vplivu
kovin potrebne.
V predstavljenem delu smo spremljali akumulacijo cinka, kadmija in bakra pri kopenskem raku
Primo` Zidar: The influence of zinc on the accumulation...  9
stevilka 1_05.qxp  13.12.2005  12:32  Page 9
enakono`cu vrste Porcellio scaber po izpostavitvi eni kovini ali pa dvem kovinam hkrati. Tovrstne
raziskave so pomembne za razumevanje kinetike kovin pri rakih enakono`cih ter za pravilno vred-
notenje okoljskih podatkov.
V poskusih smo uporabili mladi~e kopenskih enakono`nih rakov vrste Porcellio scaber, ki so bili
vzgojeni v laboratoriju. @ivali smo 21 dni hranili z listi leske (Corylus avellana), ki smo jim dodali
vodno raztopino cinka, bakra ali kadmija (Zn – 1000 in 3500 mg kg-1 suhe te`e hrane; Cu – 500 in
2000 mg kg-1 suhe te`e hrane; Cd – 250 in 500 mg kg-1 suhe te`e hrane) ali pa zmesi cinka in kad-
mija oziroma cinka in bakra. Primerjali smo koli~ino akumuliranih kovin v odvisnosti od koncen-
tracije kovin v hrani in koli~ine zau`ite hrane v ~asu poskusa.
Pri `ivalih, ki so bile izpostavljene le eni od kovin je telesna vsebnost kovin nara{~ala s koncen-
tracijo kovine v hrani. Z nara{~ajo~o koncentracijo kovin je upadala koli~ina zau`ite hrane, kar je
vplivalo na privzem kadmija, na privzem cinka in bakra pa ni imelo zna~ilnega vpliva. Akumulacija
bakra in kadmija je bila zna~ilno ni`ja ob prisotnosti cinka v hrani, medtem ko na akumulacijo cinka
prisotnost bakra ali kadmija ni vplivala. Rezultati so tako pokazali, da med cinkom in kadmijem ter
cinkom in bakrom verjetno prihaja do interakcij, zaradi ~esar se privzem kadmija in bakra zmanj{a.
Prav tako interakcije med cinkom in kadmijem ter cinkom in bakrom lahko vplivajo na kinetiko
asimiliranega kadmija in bakra zaradi ~esar je izlo~anje prese`nih koncentracij slednjih uspe{nej{e.
Omenjene ugotovitve je potrebno upo{tevati pri vrednotenju okoljskih podatkov.
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