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Accumulation and Elimination of Chromium by Freshwater

Species Exposed to Spiked Sediments


Mercedes Marchese Ana M. Gagneten
Mar a J. Parma Paola J. Pave
Received: 24 August 2007 / Accepted: 21 January 2008 / Published online: 15 February 2008
Springer Science+Business Media, LLC 2008
Abstract The bioaccumulation and elimination capacity of
chromium were examined in four freshwater species: the
submersed aquatic plant Ceratophyllum demersum (Cerato-
phyllaceae), the oligochaete Limnodrilus udekemianus
(Tubicidae), the crab Zilchiopsis collastinensis (Decapoda),
and the sh Cnesterodon decemmaculatus (Poeciliidae). All
of the species were exposed simultaneously to sediments
spiked with Cr (K
2
Cr
2
O
7
) at different concentrations for 28
days, followed by 7 days without Cr to evaluate the concen-
tration of residual Cr. We found that Cr accumulated in the
tissues of all four species. The highest bioconcentration factor
obtained for each species is as follows: C. demersum, 718.66
(272.91); L. udekemianus, 172.55(80.8), Z. collastinensis,
67.72 (35.4); C. decemmaculatus, 23.11 (12.82), all at 28
days of exposure.
Introduction
Heavy metals are highly resistant to environmental degra-
dation and can affect aquatic organisms as toxic substances
in water and sediment, or as a toxicant in the food chain,
with a strong tendency to bioaccumulate in aquatic life.
There is a substantial literature on bioaccumulation, mainly
of organic chemicals, in aquatic plants, oligochaetes, crabs,
clams and shes (Ankley et al. 1992; Conrad et al. 2000;
Egeler et al. 2004; van Hoof et al. 2001), but there is little
information on chromium (Cr) accumulation in freshwater
species (D as Correa et al. 2005; Ip et al. 2005; Nussey
et al. 2000; Su et al. 2005; Van der Putte and Part 1982).
Chromium is used in the production of steel and alloys,
pigment manufacturing, plating, wood preservation, com-
bustion of coal and oil, and leather tanning, which at higher
concentrations causes serious environmental contamination
in soil, sediments, and groundwater (Adriano 2001; Su
et al. 2005).
In natural waters two stable oxidation states of Cr persist
(III and VI), which have contrasting toxicities, motilities,
and bioavailability (Scott and Li 1996), and although at the
cellular level Cr(III) might be toxic to organisms, Cr(VI) is
the highest toxic form. This is highly soluble in water and a
strong oxidizing agent that causes severe damage to cell
membranes (Mei et al. 2002). Cr(III) is toxic because of its
ability to form complexes with nucleic acids, proteins, and
organic compounds (Su et al. 2005).
Our objective was to evaluate the bioaccumulation
potential and elimination of Cr by four freshwater species,
enlarging the set of responses measured to characterize
exposure and possible trophic transfer. Metal bioavail-
ability, as measured by metal accumulation into the tissues
of organisms, was also examined. The submersed aquatic
plant Ceratophyllum demersum (Ceratophyllaceae), oligo-
chaete Limnodrilus udekemianus (Tubicidae), crab
Zilchiopsis collastinensis (Decapoda), and sh Cnester-
odon decemmaculatus (Poeciliidae) were chosen for the
present study because these species are representatives of
the regional biota and colonize both lotic and lentic sys-
tems. They are also good candidates for use as sentinel
organisms for their sedentary habits or scarce mobility and
to belong at different trophic levels.
M. Marchese M. J. Parma P. J. Pave
Instituto Nacional de Limnolog a-INALI (CONICET-UNL),
Jose Macia 1933, 3016, Santo Tome, Santa Fe, Argentina
M. Marchese (&) A. M. Gagneten M. J. Parma
Facultad de Humanidades y Ciencias (FHUC-UNL),
Ciudad Universitaria, 3000 Santa Fe, Argentina
e-mail: mmarchese@datamarkets.com.ar
1 3
Arch Environ Contam Toxicol (2008) 55:603609
DOI 10.1007/s00244-008-9139-0
The use of multispecies tests in the current study pro-
vides important information with ecological applications
and it links toxicological effects at the individual and
community levels (Landis and Yu 1999).
Materials and Methods
In order to understand the complex ecological system, we
reproduced a model with features that simulate the structure
and function of natural systems using static mesocosms
located outdoors (3139
0
56.51
00
S- 6045
0
21.19
00
W) during
spring(SeptemberOctober 2005) toinvestigate the responses
of four species simultaneously. The tanks were covered with a
net in order to avoid the input of allochthonous material. The
water quality tested was similar to the hard water of the trib-
utaries from the right margin of the Middle Parana River
(Argentina).
The study was conducted in six PVC tanks of 1000 L
each, containing articial sediment, composed of sand,
kaolin clay, and peat (OECD 2004), and dechlorinated and
aerated tap water. The Cr-spiked sediment was placed in
each tank and overlying water was added to produce a
sedimentwater volume ratio of 1:4 (130 kg sediment and
800 L of water) and allowed to equilibrate for 5 days.
Spiked sediments of the chosen concentration were pre-
pared by the addition of a solution of the test substance
directly to the sediment. A stock solution of the test sub-
stance dissolved in deionized water was mixed with the
formulated sediment by hand mixing (OECD 2004).
Macrophytes, oligochaetes, crabs, and sh were placed
together in each tank and exposed to sediments spiked with
Cr (K
2
Cr
2
O
7
) at nominal concentrations of 3 mg Cr(VI)/L
(treatment 1, T1) and 6 mg Cr(VI)/L (treatment 2, T2),
using two replicates per concentration, and a control (T0)
under all the same conditions without the Cr.
A preliminary experiment was conducted in order to
optimize the test conditions of the denitive test [e.g.,
selection of test substance concentration(s), duration of the
uptake, and depuration phases]. The 7-day elimination
phase was governed by the period over which the con-
centration of Cr in the sh remains above the analytical
detection limit.
Ceratophyllum demersum and Z. collastinensis were
collected in uncontaminated oodplain lakes; L. udekemi-
anus were obtained from material commercially available
as sh food. They were bred in the articial sediment
(OECD 2004) at 20 2C in single-species cultures
and fed with a suspension of nely ground TetraMin

akes. C. decemmaculatus were obtained from our own


cultures.
At the end of the stabilization period, 500 g of
C. demersum, 200 g of L. udekemianus adults, 36
specimens of Z. collastinensis, and 125 specimens of C.
decemmaculatus (1.72.8 cm total length) were randomly
distributed in each tank.
Samples of water (1 L), sediment (250 g), macrophytes
(10 g of leaves), oligochaetes (23 g), gills of crabs (two to
three organisms), and sh (10 specimens pooled as a
whole-body tissue) were taken in each tank to determine
the total Cr concentration at 0, 1, 7, 14, and 28 days during
the accumulation phase and at 1 and 7 days during the
elimination phase. For this phase, the organisms were
transferred to an aquarium with clean articial sediment
and dechlorinated tap water to evaluate the concentration
of residual Cr. In both phases, a nely ground suspension
of aked sh food (TetraMin) was added every 2 days. The
temperature and dissolved oxygen were measured daily
with an oxymeter (YSI 55 model). The conductivity, pH,
and salinity were checked daily with a Horiba U10 water
meter; total hardness was checked by the titrimetric method
(APHA 2005); ammonia and Cr(VI) concentrations were
measured weekly by ultraviolet (UV)-visible spectroscopy.
An aliquot of the sediment was taken from each tank at
days 14 and 28 of the accumulation phase and centrifuged
at 4500g for 30 min, after which the pore-water supernatant
was carefully poured off for determination of Cr. For the
determination of total Cr in water and pore water, samples
were treated according to EPA Method 200.2 (US EPA
1991) and analyzed by atomic absorption spectrometry
(Perkin-Elmer AAnalyst 800, with quantication limit of
3 lg/L and detection limit of 1 lg/L). For the determina-
tion of total Cr in sediment, samples were treated according
to EPA Method 200.9 (US EPA 1991) and analyzed by
atomic absorption spectrometry, with electrothermal
atomization. Tissue samples were digested according to the
EPA Method 200.3 (US EPA 1991) and analyzed by
atomic absorption spectrometry. The oligochaetes were
separated from the sediment and kept for 56 h in water for
purging their gut contents and then the worms were rinsed
to remove any remaining debris and were frozen. The crabs
were washed with deionized water to remove adhering
particles and the metal adsorbed onto the carapace, and
they were frozen for 24 h before dissecting the gills of
individuals with a plastic scalpel and forceps.
The TOC (total organic carbon) concentration measured
in the water column was obtained by the acidic sparging
process. The procedure for AVS (acid-volatile sulde)
analysis followed the method described by Allen et al.
(1993). Calibration curves, matrix spikes, apparatus blanks,
and standard recoveries were employed in the analysis.
Duplicate measurements showed that the concentrations of
AVS were reproducible with an analytical precision better
than 10%.
A kinetic study was not performed to analyze the
equilibrium concentrations of Cr in the organisms, but,
604 Arch Environ Contam Toxicol (2008) 55:603609
1 3
generally, for most contaminants, greater than 80% of a
steady state between sediment and organisms is approa-
ched in 28 days of exposure (ASTM 1997; Ingersoll et al.
2003). Thus, the bioconcentration factor (BCF, tissue/water
ratio) and the bioaccumulation factors (BAFs, tissue/sedi-
ment ratio) were calculated at the end of a 28-day
exposure. The concept of BCF used in our study is the ratio
of a chemical concentration in an organism to the con-
centration in water and BAFs is the ratio of a chemical
concentration in an organism to the concentration in sedi-
ment. The BCF for the macrophytes, oligochaetes, crabs,
and sh were calculated according to Newman and Unger
(2003): BCF = (Ce Ci)/Cw, where Ce = metal concen-
tration in the tissue during Cr exposure [lg/g dry weight
(dw)], Ci = the initial metal concentration in the tissue
before Cr exposure (lg/g dw), and Cw = metal concen-
tration in water (mg/L). The BAFs, the relation between the
metal concentrations in the tissue and the sediment,
was also calculated for L. udekemianus as follows:
BAF = (Ce Ci)/Cs, where: Ce = Cr concentration in
tissue (lg/g dw) during Cr exposure, Ci = the initial Cr
concentration in tissue (lg/g dw) before Cr exposure, and
Cs = Cr concentration in sediment (lg/g dw). The BCF
and BAFs were expressed as a function of the total weight
of the macrophytes, worms, crabs, and sh samples.
Normality of data or log-transformed data was checked
using the Kolmogorov-Smirnov goodness-of-t test.
Analysis of variance (ANOVA) followed by the Tukey test
was used to compare mean values (a = 0.05). When data
or transformed data were not normally distributed (e.g.,
data of elimination phase), we used the nonparametric
Kruskal-Wallis test followed by a multiple-comparison test
to check for signicant differences between treatments
(a = 0.05).
Results
The AVS concentrations in the sediment were always\1.0
mg/kg dw, and the TOC ranged from 4.52 to 7.58 mg/L
(Table 1). No signicant differences were registered in
dissolved oxygen, temperature, conductivity, pH, salinity,
and ammonia during the whole study period (ANOVA
p [0.05). The ammonia concentration was relatively high
due to the organisms excretion but was below the lethal
concentration (21.4 mg/L) reported for benthic inverte-
brates by Schubauer-Berigan et al. (1995) and for
nonsalmonid sh (0.54.6 mg/L (Rand and Petrocelli,
1985).
Chromium concentrations in water and sediments
among the control and the T1 and T2 tanks showed sig-
nicant differences (p \0.001) and also between T1 and
T2 (p \0.001) (Fig. 1). The Cr concentrations decreased
in water and increased in sediment during the accumulation
phase in T2.
The Cr concentration in C. demersum, L. udekemianus,
Z. collastinensis, and C. decemmaculatus (lg/g dw)
increased rapidly, reaching the highest values between 7
and 14 days of exposure, showing that accumulation
capacity is higher in the aquatic plant and oligochaete than
in the crabs and sh (Fig. 2). It seems that the steady state
is reached between 14 and 28 days by all of the species
exposed in T2, whereas in T1, C. demersum and Z. colla-
stinensis might not have attained equilibrium after 28 days
of exposure.
The concentrations of Cr in the tissues of the macro-
phytes, oligochaetes, crabs, and sh revealed signicant
differences (p \0.05) between the control and the treat-
ments in the accumulation phase. On the other hand, the
Tukey test only showed signicant differences between the
control and T2 (p \0.05) in the macrophytes, oligochae-
tes, and sh and between both treatments (p \0.05) in
crabs. The weight of the crabs was not related to Cr con-
centration (r = 0.025). On the other hand, there were no
signicant differences in Cr concentration between female
and male tissues (p [0.05). The Kruskal-Wallis test
showed that there were no signicant differences in con-
centrations between the control and treatments during the
elimination phase (p [0.05).
During the elimination phase, the Cr concentration in all
of the species decreased immediately following the end of
the exposure period only in T1, but it then increased at the
end of this phase, except in L. udekemianus. On the other
hand, the Cr concentration decreased in the tissue of
aquatic plants and sh but not in crabs and worms at the
end of elimination phase in T2 (Fig. 2).
No dead organisms were recovered from either treat-
ments or control units.
An inverse relationship was observed between the BCF
and the exposure concentrations in all species except C.
demersum, where the plant tissue accumulation increased
in the higher concentration of Cr (Fig. 3). The highest BCF
obtained for C. demersum was 718.66 ( 272.91) in T2; for
L. udekemianus, it was 172.55 ( 80.8); for Z. collastin-
ensis, it was 67.72 ( 35.4); and for C. decemmaculatus, it
was 23.11 ( 12.82) in T1 at 28 days. The BAFs obtained
in oligochaetes was higher at 14 days than at 28 days of
exposure (Fig. 4).
Discussion
Because of their widespread release and persistent nature,
concentrations of metals such as chromium, cadmium,
copper, lead, nickel, silver, and zinc are commonly ele-
vated in aquatic sediments. These metals, in addition to
Arch Environ Contam Toxicol (2008) 55:603609 605
1 3
nonionic organic chemicals in contaminated sediments, are
a signicant pollutant source that might cause water quality
degradation to persist, even when other pollutant sources
are stopped (Burgess and Scott 1992; Ingersoll et al. 1995;
Salomons et al. 1987).
The basic routes of exposure for organisms are transport
of dissolved contaminants in pore water or water overlying
across biological membranes and ingestion of contami-
nated food or sediment particles with subsequent transport
across the gut. In this study, the high water hardness would
make the Cr less bioavailable; however, at the end of the
28-day exposure period, all of the species had bioaccu-
mulated Cr. The macrophytes, together with benthic
invertebrates (oligochaetes and crabs), showed the highest
capacity of accumulating Cr, in concentrations 50700
times higher than those found in water and participating, in
this way, in pollutant dynamics. On the other hand, the sh
showed a lower BCF (23) but higher than the BCF (\3)
reported for rainbow trout by Calamari et al. (1982).
Courdassier et al. (2005) reported for other aquatic species
(e.g., for snails) exposed to Cr a BCF of 50.8. These results
differ from the ndings of other workers who reported that
Cr did not concentrate strongly in specic tissue (Luoma
and Rainbow 2005; Pourang et al. 2004). However, the
variability in metal bioaccumulation among species is
common and Luoma and Rainbow (2005) reported that
concentrations in the tissue of different animal species
varied by seven orders of magnitude. Moreover, interpre-
tation of bioaccumulation data is complicated by the
presence of both absorbed and adsorbed forms of metals,
with the adsorbed form not incorporated into tissue but
contributing to the overall body concentration. The
L. udekemianus BAFs from sediment appear notably lower
than the corresponding BCF. This demonstrates, as repor-
ted by Egeler et al. (1999), that the extrapolation of the
BCF to other environmental compartments such as sedi-
ment is not possible. On the other hand, the BAF differs
from a BCF in that the chemical concentration in the
aquatic organism results from all possible routes of expo-
sure (dietary absorption, transport across the respiratory
surface, etc.) (Gobas and Morrison 2000).
The higher tissue concentrations were obtained in
organisms exposed to lower concentrations, so there is
probably a threshold value for different invertebrates and
sh, above which Cr incorporation is not proportional to
the exposure concentration. Similar trends was reported by
McGeer et al. (2003) and DeForest et al. (2007), who
observed for a variety of aquatic organisms an inverse
relationship between BCF and exposure concentration.
However, the plants showed a rapid uptake of Cr at higher
concentrations, which might be related to Cr toxicity
where, through broken cell membranes, plants might have
passive uptake of a large amount of the metal, as reported
by Vazquez et al. (1987) and Maine et al. (2004).
Table 1 Average values ( SD) of environmental variables measured in water (except AVS in sediment) during accumulation and elimination
phase in all the treatments
Accumulation phase Elimination phase
T0 T1 T2 T0 T1 T2
Oxygen (mg/L) 9.0 ( 0.96) 8.9 ( 0.78) 8.9 ( 0.84) 7.4 ( 0.05) 7.8 ( 0.44) 7.8 ( 0.53)
Temperature (C) 17.8 ( 2.66) 17.5 ( 2.42) 17.6 ( 2.41) 21.4 ( 1.98) 21.4 ( 1.37) 21.6 ( 1.24)
Conductivity (lS/cm) 1294 ( 69) 1219 ( 45) 1233 ( 64) 1470 ( 70) 1470 ( 50) 1480 ( 62)
pH 8.29 ( 0.13) 8.30 ( 0.12) 8.30 ( 0.12) 8.37 ( 0.05) 8.43 ( 0.09) 8.43 ( 0.09)
Salinity (%) 0.05 ( 0.00) 0.05 ( 0.00) 0.05 ( 0.00) 0.07 ( 0.00) 0.07 ( 0.00) 0.07 ( 0.00)
Ammonia (mg/NH
3
N) 0.65 ( 0.09) 1.34 ( 0.59) 1.43 ( 0.73) 0.47 ( 0.17) 0.42 ( 0.17) 0.57 ( 0.18)
Hardness (mg/L CaCo
3
) 320 ( 35.9) 295 ( 53.8) 290 ( 30.2) 281 (5.76) 307 ( 51.9) 317 ( 38.2)
AVS (mg/kg) \1.0 ( 0.0) \1.0 ( 0.0) \1.0 ( 0.0) nd nd nd
TOC (mg/L) 6.59 ( 0.81) 6.44 ( 0.70) 5.80 ( 1.09) nd nd nd
Water column Cr (VI) (mg/L) 0.02 ( 0.01) 0.27 ( 0.16) 0.90 ( 0.24) 0.04 (0.00) 0.01 ( 0.00) 0.03 ( 0.01)
Pore water (Cr mg/L) 0.003 ( 0.0) 0.003 ( 0.0) 0.006 ( 0.0) nd nd nd
nd: no determined. N = 42. T0: control, T1: treatment at 3 mg Cr (VI)/L, T2: treatment at 6 mg Cr (VI)/L
1
10
100
(days)
C
h
r
o
m
i
u
n

c
o
n
c
e
n
t
r
a
t
i
o
n
Water (mg/l) Sediment (g/g dw)
Accumulation phase Elimination phase
T1 T2 T1 T2
0 7 14 28 1 0 7 14 28 1 0 7 14 28 1
T0
1 1 1 7 7 7
T0
Fig. 1 Mean and standard deviation of the mean of Cr concentrations
in water and sediment in each treatment during accumulation and
elimination phase. Bars represent +1 SD
606 Arch Environ Contam Toxicol (2008) 55:603609
1 3
Many factors inuence the elimination of metal from the
tissues, such as temperature, pH, hardness water, age, meta-
bolic activity, and the biological half- life of the metal (Heath
1987; Holdway 1988; Larsson et al. 1985). In our study, a
rapid tendency to elimination of the accumulated Cr was
observed when the organisms were transferred to clean water;
however, the 7-day elimination phase was not enough for the
tissue depuration in all the species analyzed. Passive elimi-
nation might occur across the gills, kidneys, and integument,
and although there are differences in detoxication systems
among species, the detoxication route depends on the
physicochemical properties of the metal.
Freshwater sh can excrete a higher than normal pro-
portion of their metal intake under contaminated conditions
and thus maintain trace metal concentrations in the body at
a normal level (Leland and Kuwabara 1985). On the other
hand, Heath (1987) reported that sh can excrete metals,
and under continuous exposure to a water-borne chemical,
the excretory processes might take several hours or days to
become activated. Thus, the body burden can rise rapidly
and then actually decline somewhat with continued con-
stant exposure.
The AVSs can react with cationic metals to make insoluble
metal suldes and can thereby control pore-water metal con-
centrations (Lee et al. 2000). In this study, the AVS was\1
mg/kg and the pore-water Cr concentrations were low
(Table 1), although the Cr was available from the environ-
mental media for accumulation into benthic organisms
according to the BCF and BAFs obtained.
Many dissolved metals readily bind to dissolved (actu-
ally colloidal) organic carbon (DOC), forming complexes
that do not appear to be bioavailable (Bergman and Dor-
ward-King 1997) and metals associated with organic
matter might become available through the digestive pro-
cess (Meyer et al. 2005). However, Honeycutt et al. (1995)
have shown that metals can be stored mainly in the
digestive tracts and in the body walls of oligochaetes. In
1
10
Days exposure
u
g

C
r
/
g

d
w

u
g

C
r
/
g

d
w

u
g

C
r
/
g

d
w

1
10
100
Days exposure
1
10
100
Days exposure
C.decemmaculatus Z. collastinensis
L. udekemianus C.demersum
T0
T1
T2
0 1 7 14 28 1 7
1 7 14 28 1 7
1 7 14 28 1 7
Fig. 2 Chromiun concentrations in each freshwater species during
the accumulation and elimination phases. T0: control, T1: treatment 1
(3 mg Cr/L); T2: treatment 2 (6 mg Cr/L). The values were
transformed in x + 1
1
10
100
1000
C. decemmaculatus
B
C
F
T1
T2
C. demersum L. udekemianus Z.collastinensis
Fig. 3 Bioconcentration factor (tissue/water ratio) at 28-day Cr
exposure in both treatments. Bars represent +1 SD. T1: treatment 1 (3
mg Cr/L); T2: treatment 2 (6 mg Cr/L)
0
1
2
3
4
5
6
28
Days exposure
B
A
F
s
T 1
T 2
14
Fig. 4 Bioaccumulation factor (tissue/sediment) of L. udekemianus
at 14- and 28-day Cr exposure in both treatments. Bars represent +1
SD
Arch Environ Contam Toxicol (2008) 55:603609 607
1 3
Limnodrilus hoffmeisteri, metals are stored in rich sulfur
granules in particular cells called chloragocytes, which
form the chloragogen tissue covering the digestive tract
(Klerks and Bartholomew 1991; Klerks and Levinton
1989). Another method of detoxication occurs in oligo-
chaetes of the genus Tubifex, where the metals are stored in
the caudal part of the worm, which is eventually lost
(Lucan-Bouche et al. 1999).
The submersed aquatic plants C. demersum can act as
powerful agents of Cr removal from the environment, as
demonstrated in this study. On the other hand, Maine et al.
(2004) reported that oating macrophytes such as Salvinia
herzogii and Pistia stratiotes have the ability to absorb Cr
specically in the roots and can withstand high concen-
trations of this metal. In general, aquatic macrophytes can
have benecial effects by purifying nutrients and detoxi-
fying toxic substances (Behrends et al. 1994; Hammer and
Bastian 1989).
In Z. collastinensis, Cr increased in gills during the
detoxication phase, showing that they take part in the
elimination. Investigations of the pattern of Cr distribution
in the gills of crabs and mantle and gills of mollusks indi-
cate that Cr is deposited and immobilized at the external
surface (Dias Correa et al. 2005; Saha et al. 2005). These
organs are responsible for transferring Cr toward the
organism and take part in metal detoxication. The mech-
anism involved, which was proposed by Dias Correa et al.
(2005), is that the gills are the rst site in which Cr aggre-
gates are formed with organic molecules of glutathione,
ascorbic acid, and saccharides, forming organometallic
complexes. The crustaceans also concentrate metals in their
exoskeleton and eliminate metals via a normal physiologi-
cal phenomenon: moulting; similarly, worms use an
amputation process to adapt to contaminated media (Lucan-
Bouche et al. 1999; Ravera 2001).
Zilchiopsis collastinensis is occasionally consumed by
humans, so it could also act in the trophic transfer of Cr to
humans. Metals in invertebrate tissues also represent a
concentrated source that might be toxic in the diet of sh
(Woodward et al. 1994). Farag et al. (1999) concluded that
ingestion of metal-contaminated invertebrates might be the
principal route of metal exposure to sh.
We can conclude that all of the taxa tested in this study
accumulate Cr and might therefore be proposed as bio-
monitors of contamination of freshwater environments.
The measurements of metal concentrations in the tissues of
biomonitors reect the bioavailability of the metal in the
environment. However, C. demersum, L. udekemianus and
Z. collastinensis are better biomonitors than C. decemma-
culatus because of their higher capacity to accumulate Cr.
The 7-day elimination phase was enough to obtain a sig-
nicantly reduction of Cr by C. decemmaculatus but not for
C. demersum, L. udekemianus, and Z. collastinensis.
Acknowledgments This survey was supported by grants from the
Universidad Nacional del Litoral and Agencia para la Promocion
Cient ca y Tecnologica, Argentina (Proyect PICTO No. 13224
UNL-ANPCyT). Chromium concentrations were determinated in
Servicio Centralizado de Grandes Instrumentos (CERIDE-CONI-
CET), Laboratory in the Prociency Testing Program Canadian
Association for Environmental Analytical Laboratories (CAEL). We
also thank the International Science Editing for revising the English.
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