Cadmium-Copper Antagonism in
Seaweeds Inhabiting Coastal Areas
Affected by Copper Mine Waste
S A N T I A G O A N D R A D E ,
M A T I Ä A S H . M E D I N A ,†
J A M E S W . M O F F E T T ,‡A N D
J U A N A . C O R R E A *
Departamento de Ecologı ´a and Center for Advanced Studies
in Ecology and Biodiversity, Facultad de Ciencias Biolo ´gicas,
Pontificia Universidad Cato ´lica de Chile,
Alameda 340, Santiago, Chile
Cadmium and copper accumulation by macroalgae was
studied in a coastal area exposed to upwelling events and
high levels of Cu, the latter resulting from mine disposals.
Eight species were studied, and all had very high
concentrations of Cd outside of the Cu-contaminated
area. Cu in algal tissues was much higher in contaminated
than in reference sites. High Cu appeared to suppress
Cd bioaccumulation; Cd in algal tissues was much lower
in the Cu-contaminated area than in the reference sites.
a depuration of Cd in individuals transplanted to areas with
high Cu. However, Cd depuration occurs more slowly
than Cu uptake. These differences suggest that while Cd
Overall, the work confirms that macroalgae are useful
indicators of metal contamination and may be used as in
situ biomonitors for labile forms of metals, like free Cu2+.
However, antagonistic relationships between metals must
be clearly understood in order to properly interpret their
concentrations in macroalgae.
Cadmium is an important contaminant in coastal environ-
ments (1); it is actively accumulated by macroalgae and
invertebrates (2, 3) and, over certain levels, becomes highly
toxic to organisms. Cd is not considered a biologically
essential element, though it can be utilized in carbonic
anhydrate by phytoplankton (4). Furthermore, Cd bioaccu-
mulation in bivalves poses a potential health hazard to
humans and has important economic consequences for the
shellfish industry (5). High levels of Cd in marine organisms
Coastal upwelling areas are highly productive and have an
of benthic organisms (9), a number of which are also
in Cd-rich upwelled water off Baja California accounts for
Coastal upwellings in northern Chile are similar to those in
Baja California (13), but to date there have been no reports
of metal enrichment and bioaccumulation of Cd in marine
macroalgae from the Chilean coast.
mining operations in northern Chile, considerable work has
been done on the bioaccumulation of Cu in macroalgae in
the vicinity of the coastal mine impacted areas, including
Chan ˜aral (26°15′S; 70°40′W), where wastes from the El
Salvador copper mine have been dumped for more than 60
years, leading to excessive contamination (14). Chan ˜aral is
characterized by high levels of dissolved Cu (15), a severe
reduction in species richness with a complete modification
of the intertidal community structure (16), and high Cu
concentrations in macroalgae (14).
Despite the common occurrence of the two metals in
natural and impacted aquatic environments, the potential
relationships between Cu and Cd in macroalgae have not
of competitive interactions between different metals for
uptake, storage, and utilization documented in marine
phytoplankton (17-19), and an antagonistic relationship
between Cd and Cu uptake was recently reported (20).
In this study, we investigated the bioaccumulation of Cu
and Cd simultaneously on several species of macroalgae at
presents an ideal opportunity to study the (i) accumulation
water and (ii) Cd:Cu ratios in macroalgae. Furthermore, we
assessed the dynamics of metal accumulation using trans-
Materials and Methods
Sample Collection. Samples of macroalgae and coastal
seawater were collected simultaneously between April 2003
and January 2004, at three sites in northern Chile. Among
sampling stations (Figure 1), Zenteno (26°54.1′S; 70°48.5′W)
(26°15.8′S; 70°40.6′W), on the other hand, is located close
(<200 m) to the site where wastes are currently discharged
and high levels of total dissolved Cu have been measured
At low tide, samples of red (Ahnfeltiopsis sp., Chondrus
sp., Porphyra sp.), brown (Glossophora kuntii (G. kuntii),
and green (Ulva compressa (U. compressa) and Ulva sp.)
in each site. Samples were separated by species and im-
mediately allocated in acid-clean plastic bags at 4 °C until
included a visit to each site every other month (see Table 2).
same species and was gathered along the coast in a single
site, pooled together.
Seawater samples were collected monthly during the
period of the transplant experiment (see below). Duplicate
* Correspondingauthorphone: 56-2-3542620;fax: 56-2-3542621;
†Presentaddress: CIIMAR,CentroInterdisciplinardeInvestigac ¸a ˜o
Marinha e Ambiental, Laboratory of Ecotoxicology, Porto, Portugal.
‡Present address: Department of Chemistry, Woods Hole Oceano-
graphic Institution, Woods Hole, MA.
Environ. Sci. Technol. 2006, 40, 4382-4387
43829ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 14, 200610.1021/es060278c CCC: $33.50
2006 American Chemical Society
Published on Web 06/14/2006
samples were taken from the shore using acid-washed low-
density polyethylene bottles (1 L) secured to a 3-m non-
metallic pole sampler according to Andrade et al. (21). After
collection, bottles were placed in a double plastic bag and
kept at 4 °C until analysis.
Transplant Experiment. Transplantation of the brown
kelp L. nigrescens was set up in three steps using the
methodology described by Correa et al. (22). First, L.
nigrescens individuals of 4-8 cm holdfast diameter and up
to 120 cm frond length were simultaneously collected from
natural stands at both reference sites (Figure 1). Forty-five
receiving sites (see below). The remaining 15 plants were
fastened to the rocky platform near the place where they
were detached, as control for manipulation. These auto-
transplant groups were labeled as GG (Guanillo to Guanillo)
or ZZ (Zenteno to Zenteno), depending on the site of
the 30 individuals of each site kept in tanks, a group of 15
to Caleta Palito. During low tide, these plants were fastened
to the rock at their natural position in the intertidal zone.
These groups were labeled as GP (Guanillo to Palito) or ZP
(Zenteno to Palito).
The last step started 48 h after plants were removed from
and 15 individuals from Zenteno were cross-transplanted
and fastened in the other site (i.e. Z and G, respectively).
Between detachment and fastening of plants, the water in
the tanks was renewed every half-hour to reduce the
physiological stress of algae. These two groups were labeled
as GZ (Guanillo to Zenteno) and ZG (Zenteno to Guanillo)
Immediately after fastening to the rock, six individuals of
to determine the basal (t0) levels of Cd and Cu. At Caleta
Palito, three to six different individuals per group (GP and
ZP) were also sampled after 36 h and 1 and 2 months of
transplantation. In the sites of origin, fastened individuals
were sampled 1 and 2 months after transplantation only.
Samples consisted of 10 cm of frond tissue taken from each
plant and were maintained separately in acid-clean plastic
bags at 4 °C until analysis. The entire transplant experiment
took place from May to July 2003.
Analytical Procedure. Samples of algal tissue reached
the laboratory within 72 h of collection. Upon arrival, the
tissue was washed three times with filtered seawater,
sonicated for 30 s and oven-dried to constant weight at
45 ( 5 °C. Three subsamples of ≈0.3 g of dry alga were di-
wave oven (Milestone MLS 1200 Mega). Determination of
Cd and Cu were conducted by inductively coupled plasma
mass spectrometry (ICP-MS) in a Perkin-Elmer ELAN 6100
calculated from five replicate readings of each subsample.
wt for Cd and Cu, respectively. Analytical grade reagents
determination of total metals in algae. In both cases, the
values (“t” test, P > 0.05).
µm cellulose acetate Millipore membrane filters, with a
polycarbonate filter unit. Samples were fixed with 0.5 mL of
concentrated nitric acid (pH < 2) per liter of sample and
UV-irradiated using a Metrohm 705 UV digester. Dissolved
Cu and Cd concentrations were determined by differential
pulse anodic stripping voltammetry analysis (DPASV) using
a Metrohm 757 VA processor, following the methodology
described by Metrohm (23). The detection limits were 0.1
of the measurement procedure was checked against the
Research Institute, Canada. The metal contents were not
All pretreatment and analyses of seawater samples were
Statistical Analysis. Data were checked for normal
distribution and homogeneity of variance by application of
the Kolmogorov-Smirnov test and the Levene’s test, respec-
tively. Statistical comparisons were performed using t tests
and ANOVA procedures. In the latter, significant differences
hoc Tukey’s multiple comparison tests (24).
Cd and Cu concentrations in seawater of the three study
varied from below detection limits in Guanillo and Caleta
Palito to almost 0.2 µg L-1in Zenteno. Dissolved Cu
FIGURE 1. Study area and location of the three sampling sites (b).
Arrows indicate the transplant experiment using the brown kelp
to the site of detachment and fastening: from Zenteno to Zenteno
(ZZ), Guanillo (ZG), and Caleta Palito (ZP) and from Guanillo to
Guanillo (GG), Zenteno (GZ), and Caleta Palito (GP).
TABLE 1. Salinity and Total Dissolved Concentration of Cd and
Cu in Seawater (Mean Values ( Standard Deviation
(n ) 6))a
sitecode salinity (psu) Cd (µg L-1)Cu (µg L-1)
33.9 ( 0.5
33.7 ( 0.4
33.3 ( 0.8
0.17 ( 0.11
2.40 ( 1.52
10.69 ( 2.05
4.30 ( 2.43
aND: below detection limits.
VOL. 40, NO. 14, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY94383
among sites (one way ANOVA F(2,5)) 49.996, P < 0.05). The
post-hoc Tukey’s multiple comparison tests showed that
dissolved Cu levels in Caleta Palito were significantly higher
than both Guanillo and Zenteno, which did not differ from
Metal Concentration in Macroalgae. Algal Cd and Cu
data are shown in Table 2. The most significant finding was
of magnitude lower than in algae from the reference sites
(Zenteno and Guanillo). At this site, the lowest and highest
amounts of Cd were found in U. compressa and G. kunthii,
respectively, while the lowest Cd concentration at the
reference sites was recorded in Ulva sp. and the highest in
All macroalgal species collected at Caleta Palito showed
Cu concentrations higher than those from reference sites,
ranging from 93.5 µg g-1of dry wt in U. compressa to 1600
µg g-1of dry wt in G. kunthii. The Cu content of algae from
sp. to 27.1 µg g-1of dry wt in Porphyra sp. It is necessary to
indicate that species common to both contaminated and
reference sites displayed intermediate levels of Cu.
The Cu-to-Cd ratio varied between 0.4 and 2.6 in algae
from the reference sites and between 203 and 1052 in those
lower Cd values at that site compared with those at the
Transplant Experiment. Cd concentrations in L. nigre-
scens transplanted within (autotransplants) and between
reference sites (cross-transplants) and to Caleta Palito are
shown in Figure 2A. No significant differences in Cd levels
at t0were found between plants from Guanillo and Zenteno
(t10 ) 0.485, P > 0.05). At this time, the average Cd
concentration in these plants was 7.27 ( 1.59 µg g-1of dry
wt. After 36 h of being transplanted and exposed to the Cu-
enriched environment of Caleta Palito, Cd levels in these
maintained as controls at the reference sites (t15) 1.46, P >
decline in Cd content was observed in relation to their basal
of plants maintained at Zenteno (ZZ and GZ) and Guanillo
whereas in Caleta Palito the levels of the metal dropped to
3.4 µg g-1of dry wt in plants from Zenteno (ZP) and to 2.19
µg g-1of dry wt in plants from Guanillo (GP). Two months
after the beginning of the experiment, the Cd concentration
of the level recorded in plants maintained at the reference
In general, Cu in L. nigrescens behaved in an opposite
manner to Cd (Figure 2B). In Zenteno and Guanillo the Cu
content was <4.3 µg g-1of dry wt at t0 but increased
to Caleta Palito. After this period, the Cu concentrations in
plants from Zenteno and Guanillo reached mean concentra-
tions 7.3 and 12.7 times higher than their respective basal
TABLE 2. Ranges of Cd and Cu Content in Macroalgal Samples from the Studied Sitesa
site algal speciesN Cd (µg g-1dry wt)Cu (µg g-1dry wt)Cu/Cd
aMetal ratios, calculated from mean concentration values, are also indicated.
FIGURE 2. Cd (A) and Cu (B) content in Lessonia nigrescens fronds
determined in individuals transplanted from Zenteno to Zenteno
(ZZ), Guanillo (ZG), and Caleta Palito (ZP) and from Guanillo to
Guanillo (GG), Zenteno (GZ), and Caleta Palito (GP).
43849ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 14, 2006
levels. These differences became even more evident after 1
Palito (t4) 56.10, P < 0.01). In this case, transplants from
Guanillo and Zenteno displayed levels of Cu 24.1 and 25.5
times higher than those plants maintained at their original,
and after 2 months of exposure, transplants from Zenteno
their autotransplant controls. Cross-transplants between
changes in Cu accumulation, even after 2 months of
When metal contents of all algae analyzed in this study
correlation (r ) 0.857, P < 0.01) was found between Cd and
Cu in their tissues (Figure 3).
The results suggest that the concentrations of Cu and Cd in
phase concentrations of the metals as well as their relative
concentrations. Evidently, the uptake and/or sequestration
pathways are mechanistically linked in order to account for
these observations. In the following section, we argue that
while there are little data to provide a molecular under-
standing of these processes in macroalgae, research in
unicellular algae provides some insight and guidelines for
future research in the former group.
Cd and Cu Concentration in Macroalgae. The range of
Cd in the eight species of macroalgae from the reference
for algae in non-upwelling areas (25-28) but were within
were in agreement with values previously reported in
macroalgae from different parts of the world (26, 29, 30).
However, the high concentration of this metal measured in
for 2 months to this site, agree only with what has been
reported in marine algae from other contaminated coastal
systems (29, 31, 32).
Relationship between Dissolved Cu and Cd Concentra-
between dissolved Cu and the concentration of the metal in
the algal tissues. However, while dissolved Cu increases up
to four times (2.5-4 times) in contaminated sites, algal Cu
is that Cu accumulation is proportional to the free Cu2+ion
and simple inorganic complexes, rather than the total
dissolved concentration, which includes many complexes
that are non-bioavailable. This mechanism, included in the
so-called free ion model, has been shown to be a valuable
predictive tool for toxicity to many marine organisms,
including unicellular phytoplankton (33). Recently, we
studied the speciation of Cu at these sites using anodic
stripping voltammetry (21), and results indicated an almost
60-fold increase in free Cu2+between the pristine (0.01-
0.006 µg L-1copper in Guanillo and Zenteno, respectively)
and contaminated sites (0.33 µg L-1in Caleta Palito). This
by the elevated Cu at the contaminated site. Taking into
consideration the average values of free Cu2+(21) together
with copper levels in L. nigrescens from the transplant
experiment, harvested after 2 months of exposure to the
contaminated environment, it was found a 43-fold increase
in Cu over the initial values of the metal in the plants,
comparable to the difference in free Cu2+.
Our data suggest that the Cu content in macroalgae may
be a useful indicator of the biologically available fraction of
Cu in seawater. The rapid accumulation of Cu observed in
transplanted L. nigrescens suggests that macroalgal metal
in metal inputs may be difficult to detect with conventional
metal sampling strategies. Clearly, a calibration would need
to be performed with any given species to determine the
relationship between Cu content in the algae and dissolved
in the reference sites, are remarkably similar.
For Cd, we have no speciation data, and our study sites
show that the Cd concentration in the water was below
detection limits. However, it is highly unlikely that the
decrease of Cd in algae from Caleta Palito is due to stronger
complexation in the aqueous phase. In general Cd is weakly
complexed by organic matter, and there is no reason to
there was no significant difference in Cu binding ligands
for Cd decrease in the algae is an antagonistic interaction at
the molecular level. This is supported by the work of Wei et
al. (20), who experimentally demonstrated that metals such
as Cu, Cd, and Zn had different effects on phytochelatin
production in Thalassiosira pseudonana (T. pseudonana),
depending upon the free metal concentration in the water.
These authors suggested antagonistic relationships as the
to Cd and/or Pb in laboratory assays (34).
Variations of Cadmium and Copper Concentrations in
Macroalgae. The transplant experiment revealed that indi-
viduals exposed to the Cu-enriched environment of Caleta
Palito experience an increase in Cu content, in agreement
is the first demonstration of a concomitant decrease in Cd
content. However, Cu increase and Cd loss occurred over
of hours, while Cd decreased over a course of weeks to
months. Therefore it is not a simple displacement of one
metal for another at binding sites associated with sequestra-
tion, for example intracellullar chelators such as phytoche-
latins or metallothioneins. There are several plausible
explanations. Both metals may be sequestered by phyto-
chelatins, as has been observed in marine phytoplankton
(36). Oxidative stress associated with Cu toxicity may
FIGURE 3. Correlation between Cd and Cu content in the eight
species of naturally occurring macroalgae from Z and G (b) and
fastened in Z and G (0) and transplanted to Caleta Palito: after 36
h (/); 1 month (4), and 2 months (2). (n ) 159.)
VOL. 40, NO. 14, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY94385
consume glutathione (37), a useful intracellular antioxidant
that is also a phytochelatin precursor, leading to a gradual
decease in phytochelatin. Cu(I) forms stronger complexes
gradually decline, Cd would be affected first. In support of
this hypothesis the activation of an antioxidant metabolism
has been reported in macroalgae inhabiting sites within the
influence of the mine tailing discharge at Chan ˜aral bay (i.e.
stress caused by elevated dissolved Cu levels (37, 39).
Alternatively, Cd may be continuously effluxed from L.
nigrescens, with a turnover time on the order of months, as
demonstrated by Lee et al. (40) in Thalassiosira weissflogii
(T. weissflogii). Competition between Cu and Cd at uptake
sites would lead to an overall decrease as efflux exceeds
uptake. Although antagonistic interactions have been dem-
recently Cd-Cu antagonism (20), at present, these mech-
anisms are impossible to distinguish.
Another potential mechanism of metal sequestration
and acting as a detoxification mechanism of toxic metals
(42). Cd sequestration by PPB has been described as an
important mechanism for Cd uptake in Macrocystis pyrifera
(M. pyrifera) (25). Moreover, PPB may be a means of storing
phosphate containing high-energy chemical bonds similar
useful to the cells during periods of stress (25). If so, the
Cu-mediated oxidative stress could lead to degradation of
the PPB with the subsequent liberation of Cd.
Cu:Cd Ratios. Comparison between different species
suggests that there are probably aspects of the mechanism
of bioaccumulation common to all macroalgae. Cu bioac-
depuration of Cd in high Cu waters were common to all
The most noteworthy difference between species is the
Cu:Cd ratio. It is noteworthy that for the four species that
grow in both pristine and contaminated waters, the trends
in Cu:Cd ratios are exactly the opposite between stations.
For instance, G. kunthii has the lowest Cu:Cd ratio in the
site. These data suggest that, despite similarities between
mechanistic differences in storage and detoxification strate-
Overall, our work suggests that macroalgae-metal in-
teractions may have many characteristics in common with
promising because it suggests that robust relationships
between biomass content, physiology, and aqueous phase
ecology of metal-macroalgal interactions and further their
value to the community as contaminant indicators.
This study is part of the research program FONDAP 1501
in Ecology & Biodiversity (CASEB) Program 7. Additional
support provided by the International Copper Association
Hole Oceanographic Institution. Field and laboratory help
We deeply thank three anonymous reviewers who made
significant contributions to improve the first version of this
(1) Fo ¨rstner, U.; Wittmann, G. T. Metal pollution in the aquatic
environment; Springer-Verlag: Heidelberg, Germany, 1983
(2) Phillips, D. J. H. The use of biological indicator organisms to
monitors trace metal pollution in marine and estuarine
environmentsA review. Environ. Pollut. 1977, 13, 281-317.
(3) Wright, D. A.; Mason, R. P. Biological and chemical influences
on trace metal toxicity and bioaccumulation in the marine and
estuarine environment. Int. J. Environ. Pollut. 2000, 13, 226-
(4) Cullen, J. T.; Lane, T. W.; Morel, F. M. M.; Sheerell, R. M.
Modulation of cadmium uptake in phytoplankton by seawater
CO2concentration. Nature 1999, 402, 165-167.
(5) Wang, W. X. Interactions of trace metals and different marine
food chains. Mar. Ecol. Prog. Ser. 2002, 243, 295-309.
contamination of air, water and soils by trace metals. Nature
1988, 333, 134-139.
(7) van Geen, A.; Husby, D. M. Cadmium in the California current
system: Tracer of past and present upwelling. J. Geophys. Res.
1996, 101, 3489-3507.
(8) Takesue, R. K.; van Geen, A. Nearshore circulation during
upwelling inferred from the distribution of dissolved cadmium
off the Oregon coast. Limnol. Oceanogr. 2002, 47, 176-185.
upwelling. Ecol. Lett. 2004, 7, 31-41.
(10) Botsford, L. W.; Castilla, J. C.; Peterson, C. H. The management
of fisheries and marine ecosystems. Science 1997, 277, 509-
(11) Martı ´n,J.H.;Broenkow,W.W.Cadmiuminplankton: Elevated
concentrations off Baja California. Science 1975, 190, 884-885.
(12) Lares,M.L.;Flores-Mun ˜oz,G.;Lara-Lara,R.Temporalvariability
of bioavailable Cd, Hg, Zn, Mn and Al in an upwelling regime.
Environ. Pollut. 2002, 120, 595-608.
Orta, L.; Granados, I.; Saldivar, M.; Ortlieb, L.; Escribano, R.;
Guzma ´n, N.; Castilla, J. C.; Varas, M.; Salamanca, M.; Figueroa,
C. Influence of coastal upwelling and El Nin ˜o-Southern Oscil-
lation on nearshore water along baja California and Chile:
Shore-based monitoring during 1997-2000. J. Geophys. Res.
2004, 109, 3009-3023.
(14) Correa, J. A.; Castilla, J. C.; Ramı ´rez, M. A.; Varas, M.; Lagos, N.;
Vergara, S.; Moenne, A.; Roman, D.; Brown, M. Copper, copper
J. Appl. Phycol. 1999, 11, 57-67.
(15) Stauber, J. L.; Andrade, S.; Ramirez, M.; Adams, M.; Correa, J.
A. Copper bioavailability in a coastal environment of Northern
Chile: Comparison of bioassay and analytical speciation
approaches. Mar. Pollut. Bull. 2005, 50, 1363-1372.
(16) Medina, M.; Andrade, S.; Faugeron, S.; Lagos, N.; Mella, D.;
Mar. Pollut. Bull. 2005, 50, 396-409.
between manganese and copper on cellular manganese and
growth in estuarine and oceanic species of the diatom Thalas-
siosira. Limnol. Oceanogr. 1983, 28, 924-934.
(18) Sunda, W. G.; Huntsman, S. A. Control of Cd concentrations in
a coastal diatom by interactions among free ionic Cd, Zn, and
Mn in seawater. Environ. Sci. Technol. 1998, 32, 2961-2968.
(19) Erre ´calde,O.;Campbel,P.G.Cadmiumandzincbioavailability
to Selenastrum capricornutum (Chlorophyceae): Accidental
metal uptake and toxicity in the presence of citrate. J. Phycol.
2000, 36, 473-483.
Cd, Cu, and Zn influence particulate phytochelatin concentra-
tions in marine phytoplankton: Laboratory results and pre-
liminary field data. Environ. Sci. Technol. 2003, 37, 3609-3618.
species and suspended particulate copper in an intertidal
ecosystem affected by copper mine tailings in Northern Chile.
Mar. Chem., in press (DOI: 10.1016/j.marchem.2006.03.002).
(22) Correa, J. A.; Lagos, N.; Medina, M.; Castilla, J. C.; Cerda, M.,
Ramı ´rez, M.; Martı ´nez, E.; Faugeron, S.; Andrade, S.; Pinto, R.;
and management applications. J. Exp. Mar. Biol. Ecol. 2006,
43869ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 14, 2006
(23) Metrohm. Determination of Zn, cadmium, lead and copper by Download full-text
anodic stripping voltammetry using carbon electrodes; Applica-
tion bulletin no. 254/1 e; Metrohm Ltd.: Herisau, Switzerland,
(24) Zar,J.BiostatisticalAnalysis,4thed.;Prentice-Hall: Englewood
Cliffs, NJ, 1999.
(25) Walsh, R. S.; Hunter, K. A. Influence of phosphorus storage on
Limnol. Oceanogr. 1992, 37, 1361-1369.
(26) Leal, M. C.; Vasconcelos, M. T.; Sousa-Pinto, I.; Cabral, J. P. S.
Biomonitoring with benthic macroalgae and direct assay of
heavy metals in seawater of the Oporto Coast (Northwest
Portugal). Mar. Pollut. Bull. 1997, 34, 1006-1015.
(27) Amado Filho, G. M.; Andrade, L. R.; Karez, C. S.; Farina, M.;
Pfeiffer, W. C. Brown algae species as biomonitors of Zn and
Cd at Sepetiba Bay, Rio de Janeiro, Brazil. Mar. Environ. Res.
1999, 48, 213-224.
(28) Lozano, G.; Hardisson, A.; Gutierez, A. J.; Lafuente, M. A. Lead
and cadmium levels in coastal benthic algae (seaweeds) of
Tenerife, Canary Islands. Environ. Int. 2003, 28, 627-631.
Mar. Pollut. Bull. 1987, 18, 564-566.
structure of Lessonia spp. Hidrobiologı ´a 1999, 398/399, 375-
(31) Marsden, D. A.; DeWreede, R. E.; Levings, C. D. Survivorship
and growth of Fucus gardneri after transplant to an acid mine
drainage-polluted area. Mar. Pollut. Bull. 2003, 46, 65-73.
2001, 74, 65-85.
(33) Campbell P. G. C. Interactions between trace metals and
organisms: Critique of the free-ion activity model. In Metal
Speciation and Bioavailability in Aquatic Systems; Tessier, A.,
Turner, D. R., Eds.; John Wiley & Sons: New York, 1995; pp
(34) Vasconcelos, M. T.; Leal, M. F. Antagonistic interactions of Pb
and Cd on Cu uptake, growth inhibition and chelator release
in the marine algae Emiliana huxleyi. Mar. Chem. 2001, 75,
(35) Ho, Y. B. Zn and Cu concentrations in Ascophyllum nodosum
to an estuary contaminated with mine wastes. Conserv. Recycl.
1984, 7, 329-337.
algae. 2. Induction by various metals. Limnol. Oceanogr. 1995,
(37) Contreras, L.; Moenne, A.; Correa, J. A. Antioxidant responses
in Scytosiphon lomentaria (Phaeophyceae) inhabiting copper-
(38) Leal, M. F.; van den Berg, C. M. G. Evidence for strong copper
(I) complexation bioorganic ligands in seawater. Aquat. Geochem.
1998, 4, 49-75.
synthesis of ascorbate and activation of ascorbate peroxidase
metal enriched environments in northern Chile. Plant Cell
Environ. 2003, 26, 1599-1608.
(40) Lee, J. G.; Ahner, B. A.; Morel, F. M. M. Export of cadmium and
phytochelatins by the marine diatom Thalassiosira weissflogii.
Environ. Sci. Technol. 1996, 30, 1814-1821.
Limnol. Oceanogr. 1996, 41, 373-387.
(42) Soldo, D.; Hari, R.; Sigg, L.; Behra, R. Tolerance of Oocytis
nephrocytioides to copper: intracellular distribution and ex-
tracellular complexation of copper. Aquat. Toxicol. 2005, 71,
Received for review February 8, 2006. Revised manuscript
received April 28, 2006. Accepted May 10, 2006.
VOL. 40, NO. 14, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY94387