Marine Pollution Bulletin 50 (2005) 396–409

www.elsevier.com/locate/marpolbul

Biodiversity of rocky intertidal benthic communities associated

with copper mine tailing discharges in northern Chile
M. Medina a, S. Andrade a, S. Faugeron a, N. Lagos b, D. Mella a, J.A. Correa a,*

a
Departamento de Ecologı́a, Center for Advanced Studies in Ecology and Biodiversity, Facultad de Ciencias Biológicas,
Pontificia Universidad Católica de Chile, Casilla 114-D, Correo Santiago, Chile
b
Departamento de Ciencias Básicas, Universidad Santo Tomás, Ejercito 146, Santiago, Chile

Abstract

Copper mine tailings have been discharged around the city of Chañaral, in northern Chile, for more than 60 years. This report
summarizes a 17-month long monitoring study of species richness and biodiversity at five intertidal sites around the point of the
tailing discharge. Total dissolved copper in sites close to the point of discharge varied between 8.72 lg/l and 34.15 lg/l, showing that
there has not been a significant reduction since 1994. However, species richness has increased, suggesting a possible recovery of the
system. While diversity of sessile organisms correlates negatively with dissolved copper, diversity of mobile invertebrates did not
correlate with the metal concentration. To explain the observed results we discuss the role of algal turf interference on the distribu-
tion of mobile invertebrates at reference sites, a top-down effect caused by the absence of carnivores at impacted sites, and an avoid-
ance strategy by some species to reduce their contact with contaminated seawater.

2004 Elsevier Ltd. All rights reserved.

Keywords: Copper; Chile; Mine tailings; Intertidal biodiversity; Recovery

1. Introduction Lancellotti and Stotz, 2004). On the western slopes of

the Andes Mountains in South America, copper mining
Different sources of anthropogenic inputs of copper has historically been the most important economic activ-
to coastal zones have been reported (Lewis, 1995; Tor- ity. As a consequence, several areas of the northern
res, 2003). Copper mining activities remain as one of Chilean coast have been affected by copper mine tailing
the most significant worldwide sources of this metal into discharges (Castilla and Nealler, 1978; Vásquez et al.,
the environment due to the large volumes of released 1999; Fariña and Castilla, 2001). One of these areas is
wastes, which usually affect relatively small areas of a Chañaral Bay, which, in 1938, began to receive wastes
given ecosystem, and because, in a number of cases, from the El Salvador copper mine (Castilla, 1983). Until
these wastes have a direct impact on coastal areas, far 1975, more than 150 · 106 metric tons of untreated tail-
away from the mining operations. Copper mining ings were continuously discharged, directly affecting
wastes have caused severe and negative effects on the more than 20 km of coastline (Castilla, 1983; Paskoff
coasts of England (Bryan and Langston, 1992), Canada and Petiot, 1990). From 1976 to 1989 the discharge
(Mardsen and DeWreede, 2000; Grout and Levings, point was moved 10 km north of Chañaral Bay to Caleta
2001; Mardsen et al., 2003), Australia (Stauber et al., Palito (2616 0 S, 7041 0 W), a rocky cove that received
2001) and Chile (Castilla, 1996; Correa et al., 1999; 130 · 106 metric tons of tailings in 13 years. After the
construction of an inland sedimentation dam in 1990,
*
Corresponding author. Tel.: +56 2 3542610; fax: +56 2 3542621. sediment-free wastewaters have been channeled from
E-mail address: [email protected] (J.A. Correa). the dam to Caleta Palito at a flow rate of 200–250 l/s.

0025-326X/$ - see front matter
2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2004.11.022
 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409 397

Since 1978, studies on beach progradation and varia- during the second year of monitoring. Local currents
tions of the intertidal benthic communities around move northward in this part of the coast and, as a re-
Chañaral and Caleta Palito have resulted in more than sult, tailing sediments have accumulated in this site over
14 reports assessing the potential effects of the mine tail- time.
ings (Castilla and Nealler, 1978; Castilla, 1983; Paskoff
and Petiot, 1990; Vermeer and Castilla, 1991; Correa 2.2. Seawater analysis
et al., 1995; Castilla, 1996; Correa et al., 1996; Castilla
and Correa, 1997; Riquelme et al., 1997; Correa et al., Since copper has been reported as the main single
1999; Correa et al., 2000; Lee et al., 2002; Ratkevicius pollutant in the tailing discharge (Correa et al., 2000),
et al., 2003; Lee and Correa, 2004). From these studies we measured its total dissolved concentration in the
it is clear that the most important effects of the tailing water column around the studied sites. Two 500 ml sea-
discharges on the coastal zone around Chañaral are: water samples were collected from the shore with acid-
the persistently high copper concentrations in coastal washed polypropylene bottles, and kept at 4 C during
waters, beach progradation, and the virtual elimination transportation to the laboratory. Seawater was first fil-
of algae, several benthic herbivores and all benthic car- tered through 0.45 lm cellulose acetate Millipore mem-
nivores from the impacted area (Correa et al., 2000). brane filters, fixed with 0.5 ml concentrated nitric acid
While these studies have significantly improved our (pH < 2) and stored at 4 C for analysis. Total dissolved
understanding of the effects of mine tailings on the copper concentration (TDC) as measured by anodic
biota, they nevertheless represent static pictures of the striping voltammetry (ASV) using a Metrhom 757 VA
area, disconnected in time, where specific monitoring processor following the methodology proposed by
of temporal variation in biodiversity is absent. Further- Metrohm (2000). Analytical grade reagents were used
more, these studies have applied different methodologi- to prepare all relevant blanks and calibration curves.
cal approaches that do not allow reliable comparisons. Analytical accuracy was tested against high purity refer-
In addition, although copper has been reported as ence material provided by the National Research Coun-
the main single pollutant in the Chañaral area (Correa cil of Canada (CRM-SW). In addition we recorded in
et al., 2000), its current concentration in the surrounding situ variations in the surface temperature of coastal sea-
coastal water is not known. This situation now becomes water during the study period using a submersible data
important, as local authorities claim to have achieved a logger (Optic Stow Away Temp, ONSET Computer
reduction in mine tailing contamination, which could be Corp., USA), which was deployed and fastened to shal-
leading to a possible recovery of the biodiversity in the low subtidal rocks at three of the study sites (G, P, Z).
coastal zone of Chañaral. Dissolved oxygen and pH were also measured in situ
This study assesses the existence of (a) temporal at all of the sites using a WTW Multiline P4, Universal
variations in intertidal species richness and biodiver- meter.
sity in the rocky intertidal zone around the mine tail-
ing discharges and (b) a possible ongoing process of 2.3. Biodiversity monitoring procedures
biodiversity recovery in this coastal zone. The study
includes comparisons between historical and new data In order to determine intertidal biodiversity, two dif-
and relates this information to the concentration of ferent approaches were applied. First, species richness
total dissolved copper in the surrounding coastal was determined by one observer who walked slowly
water. along the intertidal platform for 5 min recording all algal
and invertebrate species encountered. This methodology
was applied because it has been used during previous
2. Materials and methods studies of these sites (Castilla and Correa, 1997; Correa
et al., 1999). The second approach included the use of
2.1. Study sites transects and quadrats. At each site three transects, at
least 4 m apart, were defined perpendicular to the coast,
Four sites covering 100 km of coastline around from high to low along the intertidal gradient. The sam-
Chañaral were monitored at low tide (0.23–0.30 m) pling unit, a 25 · 25 cm quadrat with a grid of 100
every two months, from February 2002 to June 2003 equally spaced intersection points, was positioned along
(Fig. 1). Among these, Guanillo (G) and Zenteno (Z) the transects as many times as it fit. Algae and sessile
were considered reference sites due to their history of invertebrates occurring beneath each intersection point,
a lack of metal pollution. Palito (P) is located 200 m and all of the mobile invertebrates inside the quadrat,
south from the current discharge point (Caleta Palito), were identified to the lowest possible taxonomic level.
and Achurra (A) is close to the old discharge site, at Complete monitoring was not performed at Guanillo
the northern extreme of Chañaral Bay. A fifth site, La and La Lancha in June 2003 due to bad weather
Lancha (L), located 5 km north of Palito, was included conditions.
398 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409

GUANILLO (25º53.77’S; 70º41.55’W)

N

LA LANCHA (26º13.20’S; 70º39.83’W)

PALITO (26º15.80’S; 70º40.63’W)

ACHURRA (26º18.43’S; 70º39.83’W)

PACIFIC OCEAN

Mine tailing canal

CHILE
CHAÑARAL CITY

ZENTENO (26º51.08’S; 70º48.55’W)

Fig. 1. Chañaral area and study sites. The discharge point of the copper mine tailing is indicated (arrow).

2.4. Data analysis during summer and winter, separately for each year
(i.e. February 2002, July 2002, January 2003, June
Significant differences in TDC between sites were 2003). Patterns of similarity in species composition were
determined considering all seawater samples taken dur- contrasted using cluster diagrams of the JaccardÕs coef-
ing the study period in a one-way (between subjects) ficient calculated for each combination of sites during
ANOVA. A post hoc TukeyÕs multiple comparison test each date. Clusters were constructed using unweighted
was applied to determine which sites were significantly average linkage methods.
different from the others (Zar, 1999). Prior to this statis- The density of mobile invertebrates was quantified
tical analysis, we checked assumptions of a normal dis- by counting all individuals inside the entire quadrat,
tribution of the data and homogeneity of variance by whereas the cover of sessile organisms (algae and sessile
application of the Kolmogorov–Smirnov test and invertebrates) was obtained as percentage cover by sum-
LeveneÕs test, respectively. Standard procedures of data ming all of the intersection points on the quadrat grid
transformation (Zar, 1999) were included when where they were present (Castilla, 1988). Density and
required. percentage cover were determined in relation to the total
The JaccardÕs coefficient of similarity (Jaccard, 1901; area and grid of intersection points, respectively, gener-
Sneath, 1957) was applied to species richness data in ated by the sum of all quadrats along each transect.
order to assess similarity in species composition between Utilizing this data of density and percentage cover, we
sites (Multi-variate Statistical Package 3.01, Kovach calculated the diversity of sessile organisms and mobile
Computing Services, UK). Similarity between sites was invertebrates for each site and date using the Shannon–
first calculated considering the presence of species for Wiener diversity index. In order to assess the level of
the entire period of study. Subsequently, similarity was occupation of primary space in each site, the percentage
determined using only the species observed at each site of bare rock was also obtained from percentage cover
 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409 399

data and plotted against time. Differences in primary Table 1

space occupation and biodiversity within each site over Mean, minimum and maximum values of total dissolved copper
concentration (TDC) considering the entire period of study
time were determined by one-way repeated measures
(within subjects) ANOVA. Sites were then compared Site Mean Minimum Maximum Number
(lg/l) (lg/l) (lg/l) of samples
on four different monitoring dates (February 2002, July
2002, January 2003 and June 2003) by a one-way (be- Guanillo 3.13 1.62 4.55 8
La Lanchaa 20.86 9.85 34.15 8
tween subjects) ANOVA. The post hoc TukeyÕs multiple Palito 17.04 8.72 25.64 10
comparison test was applied to determine which sites Achurra 7.18 6.33 9.83 6
were significantly different from the others (Zar, 1999). Zenteno 5.58 4.01 7.52 6
Prior to the first statistical analysis, we checked data Sites are listed from north to south.
for the assumption of homogeneity of covariance by a
Values correspond to analysis of samples obtained between Jan-
the application of the MauchlyÕs test of sphericity (Kin- uary and June 2003.
near and Gray, 2000). When this assumption was not ful-
filled, the more conservative Greenhouse-Geisser test
was applied (Kinnear and Gray, 2000). Assumptions of (Table 1). Since the LeveneÕs tests applied to the data
a normal distribution and homogeneity of variance were showed some violation of homogeneity of variance,
also checked prior to the second analysis, as mentioned ANOVA was performed following log-transformation
above. In order to test the degree to which TDC and of the data.
intertidal biodiversity were related, we calculated the
PearsonÕs correlation (r) (Zar, 1999). For this, we utilized 3.2. Species richness and similarity
the TDC data obtained during the entire study period,
and the corresponding diversity data (all transects) for Considering all sites and the entire study period, we
sessile organisms and mobile invertebrates. identified a total of 84 entities (Table 2). From these,
Finally, since algae were the main users of primary 63 were identified to the species level, 12 to the genus
space, the relationship between their spatial dominance evel and 8 were classified at higher taxonomic levels. A
and temporal incidence was analyzed in order to identify non-calcareous crustose alga did not fit in any taxo-
the most representative species. Mean percentage cover nomic group and, thus, remained as ‘‘green crust’’. All
considering all transects and dates were plotted against identified entities were treated as different taxa or puta-
the frequency of presence of each species during the tive species, which allowed biodiversity analysis and
entire study period. comparisons between sites.
From the 84 entities identified, 37 were algae, 15 were
sessile invertebrates and 32 were mobile invertebrates
3. Results (Table 2). It should to be noted that 19 algae and 11
invertebrate species were present exclusively at the refer-
3.1. Seawater parameters and total dissolved copper ence sites (G and Z), and only 3 algae and 2 invertebrate
species were never recorded at these sites. The phaeo-
Dissolved oxygen ranged between 8.52 and 9.05 mg/l phycean Order Scytosiphon deserves special attention,
and pH varied between 7.98 and 8.13 between all sites, as it later became clear that our initial conclusion that
but remained almost constant within each site during only S. lomentaria was present in the area had to be
the entire study period. Temperature, on the other hand, re-considered. For the purposes of this study, and based
showed the expected seasonal variation at the three con- on conclusive but still unpublished information we as-
tinuously monitored sites (G, P, Z), with values as low signed two different entities, with the status of species,
as 12 C in winter and up to 18 C in summer. to the genus Scytosiphon (Table 2). The persistently
Our results of TDC showed that concentration of this higher levels of copper recorded at the impacted sites
metal continues to be significantly higher (p < 0.001) at were associated with a clear decrease in the total number
those sites near to the current tailing discharge (P and of species (Fig. 2A). Considering the entire study period,
L) than in the non-impacted sites (G and Z) (ANOVA, the number of species recorded in Guanillo and Zenteno
F4,37 = 23.49). The post hoc TukeyÕs multiple compari- was 67 and 75, respectively, contrasting with the 47 and
son test however, demonstrated no significant differ- 42 recorded in Achurra and Palito, respectively. Overall,
ences between any of these sites and Achurra (A), less than half of the species recorded at the control sites
where TDC values fall between those measured at the were found at their impacted counterparts at the end of
other sites. Thus, the sequence of mean TDC concentra- the study period. It is worth mentioning that the magni-
tions measured in this study was La Lancha > Pal- tude of the difference was not clear at the beginning of
ito > Achurra > Zenteno > Guanillo (Table 1). It is the study, particularly for Achurra (Fig. 2A). Species
also clear that values of TDC experienced the widest richness at the fifth site, La Lancha, was initially lower
fluctuations in those sites nearer to the discharge point than at the two other impacted sites, with a total of 32
400 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409

Table 2
List of species (or entities classified at the lowest possible taxonomic level) observed at the studied sites considering the entire period of study
Species G L P A Z
Algae
Chlorophyta
Ulva compressa X X X X X
Ulva linza X
Rama novaezelandiae X
Codium dimorphum X X
Codium fragile X
Ulva sp. X X X X X
Chaetomorpha sp. X
Cladophoropsis sp. X X
Rhodophyta
Porphyra columbina X X X
Polysiphonia paniculata X X X X
Corallina officinalis X X X
Gelidium chilense X X
Hildenbrandia lecanellieri X X X X X
Centroceras clavulatum X
Chondrus canaliculatus X X
Bangia atropurpurea X X X
Ahnfeltiopsis durvillaei X X
Ahnfeltiopsis furcellata X X X
Grateloupia doryphora X X
Corallina sp. X X
Lithothamnium sp. X X X X X
Mesophylum sp. X X
Gelidium sp. X X
Rhodoglossum sp. X X
Ceramium sp. X
Phaeophyta
Ralfsia confusa X X
Glossophora kunthii X X X X
Scytosiphon sp1 X X X
Scytosiphon sp2 X X X
Hincksia mitchelliae X X X
Halopteris hordacea X X X X
Lessonia nigrescens X X
Petalonia fascia X X
Colpomenia sinuosa X X X
Ectocarpus sp. X X X X X
Others
Cyanophyceae X X
‘‘Green crust’’ X X X X X

Invertebrates
Sessiles
Jehlius cirratus X X X X X
Notochthamalus scabrosus X X X X
Balanus laevis X X X X
Balanus flosculus X X
Austromegabalanus psittacus X X X
Semimytilus algosus X X X X X
Perumytilus purpuratus X X X X
Phymactis clematis X X X X X
Anthothöe chilensis X X X
Phymanthea pluvia X X X X X
Bunodactes sp. X X X X X
Porifera X X X X
Ectoprocta X X X
Spirorbidae X X X
Phoronidae X X
(continued on next page)
 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409 401

Table 2 (continued)
Species G L P A Z
Mobiles
Nodilittorina peruviana X X X X X
Nodilittorina araucana X X X X X
Scurria scurra X X
Scurria zebrina X X X X X
Scurria ceciliana X X X X X
Scurria araucana X X X X
Scurria bohemita X X X
Scurria parasitica X X X X X
Scurria viridula X X X X X
Siphonaria lessoni X X X X X
Trimusculus peruvianus X X
Fissurella crassa X X X X X
Fissurella limbata X X X X X
Fissurella maxima X X X
Concholepas concholepas X X X X X
Nucella crassilabrum X
Leptograpsus variegatus X X X X X
Taliepus dentatus X X
Loxechinus albus X X
Tetrapygus niger X X
Enoplochiton niger X X
Acanthopleura echinata X X X
Heliaster helianthus X X
Meyenaster gelatinosus X
Tegula atra X X
Stichaster striatus X X
Chiton granosus X X
Acanthocyclus gayi X X X
Betaeus sp. X X X X
Amphipoda X X X X X
Acarina X X X
Polychaeta X X

species recorded during the three sampling dates (Fig. 3.3. Bare rock and diversity of algae and sessile
2A). When algal species richness was analyzed sepa- invertebrates
rately, similar but more pronounced differences between
reference and impacted sites became apparent (Fig. 2B). Mean percentage of bare rock varied during the study
Although species richness of invertebrates was also gen- period (Fig. 4). However, repeated measures ANOVA
erally higher at non-impacted sites (Fig. 2C), differences performed independently on data from each site indi-
with those sites nearer to the tailing discharge were cated no significant differences (p > 0.05) between mon-
small, reaching similar values at different times during itoring dates for any site. Comparisons of percentage of
the study period. bare rock between sites were significantly different
Considering the entire period of study, we were able (p < 0.05) for all monitoring dates analyzed (Table 3).
to distinguish two main groups with less than 45% sim- A post hoc TukeyÕs multiple comparison test, however,
ilarity from the analysis of species composition (Fig. demonstrated no significant differences between refer-
3A). The first group (cluster 1 in Fig. 3A) was com- ence sites (G and Z), but significant differences between
prised of the two non-impacted sites and the second these two reference sites and Palito for all monitoring
group (cluster 2 in Fig. 3A) included the three impacted dates, with the exception of February 2002, when Zent-
sites. Within the latter group, La Lancha was slightly eno did not differ significantly from Palito (Fig. 4). In
different from Palito and Achurra (cluster 3 in Fig. February 2002, Achurra also showed no significant dif-
3A). When species composition was analyzed sepa- ferences with the control sites; however, it did differ
rately for summer and winter, the level of similarity be- from control sites on all monitoring dates performed
tween groups was reduced (Fig. 3B–E). However, after February 2002. During the last two analyzed dates,
similarity between sites remained relatively constant the percentage of bare rock at Achurra showed no sig-
through time (25%), and thus, the two distinct groups nificant differences with Palito. The fifth site, La Lan-
(i.e. impacted and non-impacted sites) remained clearly cha, showed no significant differences with any other
identifiable. site during the dates on which it was analyzed.
402 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409

Palito and Achurra. In January 2003, due to a drop

50
Total species (A)
in diversity at Zenteno coupled with an increase in
diversity at Palito, no differences were observed. After
40 this monitoring date, some evidence of differentiation
was observed, but statistical analyses did not detect
significant differences (Table 3). The high and signifi-
30
cant (p < 0.001) negative correlation between TDC
and diversity of sessile organisms is clearly shown in
20 Fig. 6.
Spatial dominance and incidence of algal species
10
showed important differences between sites (Fig. 7).
Guanillo and Zenteno had more than 11 algal species re-
30 corded at least 8 times during the study period, and the
Algae (B) red alga Hildenbrandia lecanellieri displayed the highest
25 incidence at both sites. In Guanillo, Ulva sp. and Litho-
thamnium sp. were reported the same number of times.
20
In terms of dominance, Ahnfeltiopsis furcellata and Ulva
Number of species

15
sp. had the highest mean percentage cover in Guanillo
and Zenteno, respectively. The red alga Centroceras cla-
10 vulatum was also important at the two reference sites,
although it had a low incidence (recorded less than 6
5 times). As indicated above, the percentage of bare rock
was high in Palito and, as a consequence, the incidence
0
and dominance of algal species was low (Fig. 7). Only
30
four species appeared more than eight times during the
(C) study which, ranked from high to low incidence, were:
Invertebrates
Scytosiphon sp2, Ulva compressa, Porphyra columbina
25
and Ulva sp. When present, U. compressa also had the
highest algal dominance. Algal incidence in Achurra
20
was similar to that in non-impacted sites; however, dom-
inance as mean percentage cover was lower. In addition,
15 in terms of incidence, U. compressa was also important
at this site.
10

5 3.4. Diversity of mobile invertebrates

Jan/2002 May/2002 Sep/2002 Jan/2003 May/2003
Monitoring dates Although variation of mobile invertebrate diversity
was not significant (p > 0.05) within monitoring dates
Guanillo Lancha Palito Achurra Zenteno at any of the sites, a different situation was observed
Fig. 2. Temporal variation in species richness. (A) Total number of when comparisons were performed between sites (Fig.
species; (B) Species of algae; (C) Species of invertebrates. 8). Mean diversity index obtained from Guanillo was
lower than that obtained from Achurra and Palito dur-
ing the entire study period. Achurra had the highest
mean index throughout the study period, with the excep-
Although the mean diversity of sessile organisms, tion of April 2003, when the indices obtained from Zent-
including algae and sessile invertebrates, ranged from eno and La Lancha were higher. When a one-way
0.79 to 0.97 at reference sites and from 0.47 to 0.75 ANOVA was used to test differences between sites, sig-
at Palito (Fig. 5), variations in time were not signifi- nificant differences were found only in July 2002 (Table
cant at any site (p > 0.05). Comparisons between sites 3), when the diversity of mobile invertebrates in Achurra
showed significant differences only in February 2002 was similar to that of Palito and Zenteno, but not to
and July 2002 (Table 3). In February 2002, the post that estimated for Guanillo (post hoc TukeyÕs multiple
hoc TukeyÕs multiple comparison test indicated signifi- comparison test). In contrast to the diversity of sessile
cant differences between Palito and all other sites (Fig. organisms, no correlation between TDC in coastal
5). In July 2002, significant differences were observed seawater and diversity of mobile invertebrates was
between Palito and reference sites, but not between observed (Fig. 9).
 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409 403

All seasons
(A) A
3
P 2

Z
1
G

0.4 0.5 0.6 0.7 0.8 0.9 1

summer 2002 winter 2002

A
(B) A (C)
3
3
P
P

Z Z

1
1

G G

0.04 0.2 0.36 0.52 0.68 0.84 1 0.04 0.2 0.36 0.52 0.68 0.84 1

summer 2003 winter 2003

(D) A (E) Z 1
3
P 2
A

L 3

P 2
Z
1
G
L

0.04 0.2 0.36 0.52 0.68 0.84 1 0.04 0.2 0.36 0.52 0.68 0.84 1

Jaccard’s Coefficient
Fig. 3. Cluster analysis of the similarity in site species composition. (A) Data considering the entire study period; (B) Data from February 2002; (C)
Data from July 2002; (D) Data from January 2003; (E) Data from June 2003. G: Guanillo, L: La Lancha, P: Palito, A: Achurra and Z: Zenteno.

100
4. Discussion
a

80
a
a a
a The study presented here summarizes data obtained
after 17 months of regular monitoring at five rocky inter-
ab tidal sites around the point of discharge of copper mine
a
60 tailings in northern Chile. Results show high and vari-
Bare rock (%)

ab ab able TDC concentrations in the coastal seawater from

b Palito and La Lancha, the closest sites to the current dis-
40 b
b charge of the waste waters from the copper mine El Sal-
b vador. Our results agree with previous information
20 c b reported by Correa et al. (1996) and Castilla and Correa
c
(1997) who attributed this variability to the potential
contribution of other small-scale operations scattered
0
Jan/2002 May/2002 Sep/2002 Jan/2003 May/2003
downstream from the mine which could illegally dis-
charge additional copper-containing wastes into the
Monitoring dates canal before it reached the sea. This certainly is not
Guanillo Lancha Palito Achurra Zenteno the situation today, as all small-scale operations have
Fig. 4. Percentage of bare rock. Values represent the mean ± SD from been dismantled. However, regardless of the eventual
three replicates. Letters indicate significant differences between sites. occurrence of copper-containing wastes added to the
404 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409

Table 3 1.2
Summary of one-way (between subjects) ANOVA performed on: (I) r = -0.61
percentage of bare rock, (II) diversity of sessile organisms (Shannon n = 51
p < 0.001
index, H 0 ), and (III) diversity of mobile invertebrates (Shannon index, 1.0
H 0 ) between sites on different monitoring dates
Site Source df MS F P

Shannon index (H’)

0.8
February 2002
I Site 3 789.88 5.49 0.03
Error 7 0.6
II Site 3 8.63 · 102 10.97 0.005
Error 7
III Site 3 8.58 · 102 2.38 0.16
0.4
Error 7
July 2002
I Site 3 1940.86 33.82 0.001 0.2
Error 7 0 5 10 15 20 25
II Site 3 8.41 · 102 6.27 0.02 Total dissolved copper concentration (µg/l)
Error 7
III Site 3 8.99 · 102 6.32 0.02 Guanillo Lancha Palito Achurra Zenteno
Error 7
Fig. 6. Correlation between total dissolved copper (TDC) in coastal
January 2003 seawater and diversity of sessile organisms (algae and sessile inverte-
I Site 4 2377.49 13.87 0.001 brates). All monitoring dates and diversity data obtained were
Error 9 included in the analysis, with the exception of the highest value of
II Site 4 2.92 · 102 3.02 0.09 TDC measured in seawater during the study period (34.15 lg/l, see
Error 8 Table 1), since diversity was not determined when this value was
III Site 4 9.57 · 102 3.99 0.05 obtained.
Error 8
June 2003
I Site 2 2279.17 41.91 0.001
discharge point have decreased significantly in recent
Error 5 years, from 2416.2 lg/l in 1995 (Correa et al., 1996) to
II Site 2 7.17 · 102 5.40 0.06 31.4–71.7 lg/l in 2003 (this study, data not shown).
Error 5 Thus, even though the canal remains as a persistent
III Site 2 1.89 · 103 0.04 0.96 source of copper to the coastal environment, its impact
Error 5
seems to be reduced in comparison to other sources, all
of which are related to copper mining activities. Today,
re-suspension of old coastal sediment deposits is likely
1.2 the most important source of copper to the water col-
umn. This is supported by two recent studies of inter-
1.0
tidal and shallow subtidal sediments present on
beaches in the area under the influence of the mining
a a a
waste products. The first study (Lee et al., 2002) demon-
Shannon index (H’)

a a
a
0.8 a a
a a
strated that, while labile copper in the water was be-
ab
a tween 10 and 50 lg/l depending on the site, the
effective copper concentration in the sediment was al-
0.6 a
a ways greater than 100 lg/l and, in some cases, greater
b
than 1000 lg/l. The second study (Ramı́rez et al., in
b
0.4 press) confirmed that copper is the main metal in the
sediments of the beaches affected by the mining wastes,
and demonstrated that an important fraction is found in
0.2
Jan/2002 May/2002 Sep/2002 Jan/2003 May/2003
a labile form, easily released from the sediment to the
Monitoring dates water column—and available to the biota. This informa-
tion regarding the availability of copper in the environ-
Guanillo Lancha Palito Achurra Zenteno
ment, together with factors that could modulate the
Fig. 5. Diversity of sessile organisms (algae and sessile invertebrates). levels of copper in the water (e.g. strong wave action
Values represent the mean ± SD from three replicates. Letters indicate and high currents that affect the study area, particularly
significant differences between sites.
during winter storms, and atmospheric dry deposition of
fine particles from the copper mine tailing beaches), may
canal before reaching the sea, it is clear that the levels of be the cause of the temporal variability observed in
total dissolved copper in the waste water before the TDC concentrations.
 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409 405

25 1 Hildelbrandia lecanellieri
25 1 Scytosiphon sp2
2 Ulva sp. 2 Ulva compressa
Guanillo 3 Lithothamnium sp. Palito 3 Porphyra columbina
4 Porphyra columbina 4 Ulva sp.
20 20
Algal incidence (# of transects where it was recorded)

5 Corallina officinalis 5 Scytosiphon sp1

3 2 1 6 Ralfsia confusa 6 Bangia atropurpurea
4 7 Lessonia nigrescens
8 Rhodoglossum sp.
5
15 8 7 6 9 Ahnfeltiopsis furcellata 15 1
10 Grateloupia doryphora
11 Ahnfeltiopsis furcellata 3 2
12 Centroceros clavulatum
10 10
11 10 9 4
5

5 5 6

0 0
0 10 20 30 40 0 10 20 30 40

25 1 Hidelbrandia lecanellieri 25 1 Hildelbrandia lecanellieri

2 Ulva compressa 2 Ulva sp.
Achurra 3 Scytosiphon sp1 Zenteno 3 Gelidium chilense
2 1 4 Ectocarpus sp. 4 Porphyra columbina
20 5 Ulva sp. 20 1 5 Ralfsia confusa
6 Scytosiphon sp2 6 Lessonia nigrescens.
4 3
7 “green crust” 4 3 7 Lithothamnium sp.
2
5 8 Porphyra columbina 8 “green crust”
15 6 7 9 Lithothamnium sp. 15 7 6 5 9 Polysiphonia paniculata
10 Corallina officinalis
11 Rhodoglossum sp.
8 12 Rama novaezelandiae
11 10 9 8 13 Ahnfeltiopsis furcellata
10 10
9 12 14 Centroceros clavulatum

14
5 5

0 0
0 10 20 30 40 0 10 20 30 40

Cover (mean%) Cover (mean%)

Fig. 7. Representation of the relative importance of algal species. Numbers have been assigned to species that were recorded more than eight times
and to species with an important contribution to cover.

1.0
r = 0.18
0.8 n = 51
0.8
p < 0.05
a
a
0.6 a
Shannon index (H’)

a a
Shannon index (H’)

0.6
a a
a
0.4 a a
a
ab 0.4

a a
0.2
a 0.2
b

0.0 0.0

Jan/2002 May/2002 Sep/2002 Jan/2003 May/2003

0 5 10 15 20 25
Monitoring dates Total dissolved copper concentration (µg/l)
Guanillo Lancha Palito Achurra Zenteno
Guanillo Lancha Palito Achurra Zenteno
Fig. 8. Diversity of mobile invertebrates. Values represent the
mean ± SD from three replicates. Letters indicate significant differ- Fig. 9. Correlation between total dissolved copper (TDC) in coastal
ences between sites. seawater and diversity of mobile invertebrates. All monitoring dates
and diversity data obtained were included in the analysis, with the
exception of the highest value of TDC measured in seawater during the
study period (34.15 lg/l, see Table 1), since diversity was not
When historical data are considered (Table 4), it can
determined when this value was obtained.
be seen that some of the TDC values obtained from Pal-
ito during this study were the lowest since this site was
first studied in 1994. The mean TDC concentration, mine tailing discharges in northern Chile (Fariña and
however, remains within the historical range and within Castilla, 2001). It has to be emphasized that the values
the range reported for other sites affected by copper reported here for Palito are measurements made in
406 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409

Table 4 Table 5
Historical data of total dissolved copper (TDC) concentrations at Historical data on species richness in Palito and La Lancha
Palito
Year Algae Invertebrates Total Reference
Year Mean Min. Max. Reference
Palito
(lg/l) (lg/l) (lg/l)
1976–1994a 5 1 6 Castilla (1996)b
1994 – 26.8 31.8 Castilla (1996)a 1996 6 11 17 Castilla and Correa
1994 29.3 25.7 32.9 Correa et al. (1995)a (1997)b
1995 14.13 – – Correa et al. (1996) 1995–1999 6 15 21 Correa et al. (1999)
1995 – 10.0 40.7 Castilla and Correa (1997)a 2003 14 28 42 This study
1996 – 10.2 13.9 Castilla and Correa (1997)a
La Lancha
1999 30.0 29.3 30.7 Correa et al. (1999)
1976–1994a 5 1 6 Castilla (1996)b
2000 14.1 – – Correa et al. (2000)a
1996 4 5 9 Castilla and Correa
2002 – 10 20 Ratkevicius et al. (2003)
(1997)b
2003 17.04 8.72 25.64 This study
1995–1999 5 6 11 Correa et al. (1999)
a
Fifty meters south of the discharge point at Caleta Palito. 2003 10 22 32 This study
a
Presence assessed by at least five consecutive or non-consecutive
observations.
water samples from 200 m south of the current dumping b
Fifty meters south of the discharge point at Caleta Palito.
site. Directly at the point of discharge point, however,
values as high as 54 lg/l and 88 lg/l were reported in
1986 and 1995, respectively (CIMM, 1996). Although due to different monitoring efforts and observer experi-
values of TDC measured at La Lancha were lower than ence in data collection must be considered when inter-
those previously reported by Correa et al. (1999), they preting results from different studies. Historical
were higher than those from Palito. According to this, differences in species richness could also be attributed
La Lancha continues to be the coastal site around to the time of the year when monitoring was carried
Chañaral with the highest level of TDC, and one of out. The present study showed that similarity between
the most copper-polluted coastal sites in the world (see sites varied in time and, when data from a particular
review by Lewis, 1995). As indicated in previous reports month was considered, it was lower than when data of
(CIMM, 1996; Correa et al., 1999), the high TDC val- the entire study period was included in the analysis.
ues at this site could reflect the influence of northward Therefore, sound estimations of species richness recov-
coastal currents on tailing dispersal and the aforemen- ery based on comparisons with reference sites will likely
tioned re-suspension of old tailing sediments by wave depend on the time of the year when the study is per-
action. From the information provided by our study formed and the length of time which the study considers.
we conclude that there has not been a significant reduc- In order to reduce the potential variability resulting
tion in the level of copper in the coastal marine environ- from the application of different visual efforts and differ-
ment affected by the mine tailing discharges in Palito, in ent observer experience during sampling, the present
comparison with the levels reported in 1994. study applied the additional, objective methodology of
Despite this first conclusion, and also considering his- predefined transects and quadrats to assess biodiversity.
torical data, the number of intertidal species in Palito By utilizing this methodology species richness deter-
and La Lancha has increased considerably during this mined by visual monitoring varied during the year, but
period (Table 5). The increase was observed in algal as the biodiversity of sessile organisms and primary space
well as invertebrate species, leading to a total species occupation (i.e. the opposite of the percentage of bare
richness 2.5 and 3.6 times higher than the values ob- rock) did not change significantly at any site. Since the
served in June 1996 in Palito and La Lancha, respec- biodiversity index applied here considers both species
tively (Castilla and Correa, 1997). Although the richness and evenness (Krebs, 1972), any temporal in-
present study coincides with the reports included in crease in the number of species observed at these sites
Table 5, regarding the pattern of species richness decline is counterbalanced by the dominance of a few species.
towards most impacted sites (Palito and La Lancha) and In contrast, any reduction in the number of species is
an increase in the number of species with time, conclu- counterbalanced by an enhanced species evenness.
sions about a possible biological recovery of the area In relation to the differences between sites, the lower
must be made with caution. This caveat is given since mean diversity of sessile organisms observed at impacted
comparisons with previous studies at the reference sites sites using transects and quadrants is consistent with the
also show a current increase of species richness. This information obtained from the visual monitoring. In this
observation suggests that the increase in species richness context, the fact that significant differences were found
around Chañaral could be the result of a more general, only during the first year of monitoring supports the
large-scale phenomenon that is not necessarily related to possibility of an ongoing process of biodiversity recov-
a reduction in the toxicity of the coastal water around ery at these sites. This is also in agreement with the
the mining discharges. Moreover, possible variability lack of significant differences in diversity of mobile
 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409 407

invertebrates between reference and impacted sites dur- detect these differences, their effects can nevertheless be
ing most of the study period. However, lower mean profound. For instance, the absence of high-level carni-
diversity values at reference sites are not consistent with vores in Palito and La Lancha, such as the starfishes
the general trends obtained here and elsewhere (Castilla, Heliaster helianthus and Meyenaster gelatinosus, could
1996; Castilla and Correa, 1997; Correa et al., 1999). As reduce predation pressure at these sites and, thus, foster
indicated above, both species richness and species even- the development of larger populations of a more herbi-
ness are considered in the biodiversity index applied in vore species. Thus, although quantitative estimators
our study. Thus, if we accept that the number of species suggest that diversity seems higher at these sites, a qual-
determined by transects and by visual monitoring is itative analysis of the intertidal assemblage of organisms
truly representative of the situation in each site, species reveals a simplified community structure. In undisturbed
evenness then becomes responsible for these unexpected intertidal sites, on the other hand, it is expected that
results. This is the result of dominance by only a few of these carnivore species directly regulate the abundance
the numerous species recorded at the reference sites, of herbivores (i.e. Dayton et al., 1977; Tokeshi et al.,
combined with a high species evenness at the impacted 1989; Espoz and Castilla, 2000) and indirectly regulates
sites, despite the presence of fewer species. This pattern algal abundance through a top-down effect (Hunter and
may be real, or could result from biased data recording Price, 1992; Correa et al., 2000). In terms of species rich-
that is intrinsically associated with the applied method- ness, the absence of the kelp Lessonia nigrescens may
ology. High algal cover at the reference sites, where a also have a strong effect. Indeed, L. nigrescens is consid-
thick algal turf is formed, may limit the primary space ered a bioengineer (sensu Jones et al., 1994) due to the
available for mobile invertebrates, interfering with their rich diversity of organisms living within its holdfast
homogenous distribution on intertidal platforms. In this (Vásquez and Santelices, 1984) and to the effect of the
case, although most mobile invertebrates could be re- frond canopy on the removal of mobile invertebrates,
corded during both the visual monitoring and counted allowing the recruitment of understory algal species
inside the quadrats, only those individuals able to move (Santelices and Ojeda, 1984). For example, Vásquez
within or above the algal turf were registered. In con- and Santelices (1984) found up to 49 species of macro-
trast, at the Palito study site algal cover is low and, thus, invertebrates living in a total of 79 sampled holdfasts,
the fewer species present are homogenously distributed with 7–15 species per holdfast. Thus, although species
in space, and easily recorded. diversity associated to L. nigrescens holdfasts was not
Two alternative hypotheses could help to understand estimated in the control sites, the absence of this kelp
the higher diversity of mobile invertebrates at the im- at impacted sites is likely to be accompanied by the ab-
pacted sites. First, high diversity levels of mobile inver- sence of a significant number of invertebrate and algal
tebrates in Palito could reflect a toxicity avoidance species.
strategy. Animals that recruit to this site may tend to Finally, characterization of the diversity of mobile
move toward the upper levels of the intertidal zone in invertebrates by means of species richness and evenness
order to reduce their contact with copper-enriched sea- (Shannon–Wiener) has not been reported previously in
water. This would result in easier recording of mobile this area nor other areas impacted by copper mine tail-
invertebrates by both visual and quadrat monitoring in ing discharges in northern Chile. Therefore, this study
Palito, as compared to the reference sites, where animals represents the starting point for future assessments of
remain at lower intertidal and shallow sub-tidal levels. biodiversity at these impacted areas. However, it is
This avoidance strategy could reduce the possible detri- important to highlight the need for testing the ecological
mental effects of TDC on mobile invertebrates and, thus, and ecotoxicological hypotheses mentioned above prior
community parameters such as species abundance and to reaching final conclusions regarding past and current
richness should be independent of the level of copper effects of the copper mine wastes on the biota, as well as
enrichment in the surrounding coastal seawater. This on potentially ongoing recovery processes.
hypothesis was supported by the correlation analysis
performed using the data obtained in this study, where
no relationship was found between these two variables. 5. Conclusions
On the other hand, sessile organisms like algae and ses-
sile invertebrates are not able to avoid the possible ef- This study indicates that there has not been a signif-
fects of copper in the water and, thus, a negative icant reduction of the total dissolved copper concentra-
relationship such as the one revealed by the correlation tion (TDC) at the coastal zone around Chañaral since
analysis, should exist between the diversity of sessile 1994, in spite of the drastic reduction of the concentra-
organisms and TDC in seawater. Second, the absence tions of this metal in the water discharges. High TDC
of some keystone species at the impacted sites may be values were observed in Palito and especially in La
considered as a clear-cut difference with the control sites, Lancha, which remains as the most impacted site. How-
and although standard statistical comparisons may not ever, levels of TDC at the contaminated sites are highly
408 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409

variable in time, probably due the re-dissolution of the Castilla, J.C., Correa, J.A., 1997. Copper tailing impacts in coastal
metal from old tailing sediments deposited in the area ecosystem of northern Chile: from species to community responses.
In: Moore, M.R., Imray, P., Dameron, C., Callan, P., Langley, A.,
which are re-suspended by coastal currents and wave ac- Mangas, S. (Eds.), Copper-Report of an International Meeting.
tion and due to atmospheric dry deposition from the South Australian Health Commission National Environmental
tailing beaches. Despite the lack of a recent reduction Health Forum Monograph. Openbook Publishers, Australia, pp.
in TDC, our study showed an increased species richness 81–92.
which, in turn, suggests the occurrence of a recovery Castilla, J.C., Nealler, E., 1978. Marine environmental impact due to
mining activities of El Salvador copper mine, Chile. Marine
process at the impacted area. However, this result must Pollution Bulletin 9, 67–70.
be considered with reservation since species richness var- CIMM1996. Evaluación de impacto ambiental en la zona costera de
ies with time at both the impacted and reference sites Chañaral: Evaluación de impacto ambiental de la depositación de
and, thus, the results of comparisons between these sites, relaves en la zona costera de Chañaral y proposición y evaluación
and with historical data, are influenced by the time of de un Plan de descontaminación y medidas de mitigación, vol. 2.
Proyecto P-935112. Centro de Investigación Minera y Metalúrgica,
the year when the studies were performed. On the other Chile. p. 272.
hand, biodiversity indices did not vary with time, sug- Correa, J.A., González, P., Sánchez, P., Muñoz, J., Orellana, C., 1995.
gesting a counterbalance between these two community Copper-algae interactions: inheritance or adaptation? Environ-
parameters (i.e. richness and evenness) at all sites. Our mental Monitoring and Assessment 40, 41–51.
results also showed a lower mean diversity of mobile Correa, J.A., Ramı́rez, M., Fatigante, F., Castilla, J., 1996. Copper,
macroalgae and the marine environment. The Chañaral Case in
invertebrates in the reference sites, which could repre- Northern Chile. In: Björk, M., Semesi, A., Pedersén, M., Bergman,
sent a true pattern or may be a biased result associated B. (Eds.), Current Trends in Marine Botanical Research in the East
with the practical limitations of the applied methodol- African Region. Ord & Vetande, Uppsala, Sweden, pp. 99–129.
ogy. If this methodology is to be used in the future for Correa, J.A., Castilla, J.C., Ramı́rez, M., Varas, M., Lagos, N.,
biodiversity assessments at these or other impacted sites, Vergara, S., Monee, A., Román, D., Brown, M., 1999. Copper,
copper mining tailings and their effects on marine algae in northern
this situation needs to be clarified through additional Chile. Journal of Applied Phycology 11, 57–67.
testing of complementary ecological and ecotoxicologi- Correa, J.A., Ramı́rez, M., de la Harpe, J., Román, D., Rivera, L.,
cal hypotheses. 2000. Copper mining effluents and grazing as potential determi-
nants of algal abundance and diversity in northern Chile.
Environmental Monitoring and Assessment 61, 265–281.
Dayton, P., Rosenthal, R., Mahen, L., Antezana, T., 1977. Population
Acknowledgments structure and foraging biology of the predaceous Chilean asteroid
Meyenaster gelatinosus and the escape biology of its prey. Marine
This study is part of the research program FONDAP Biology 39, 361–370.
Espoz, C., Castilla, J.C., 2000. Escape responses of four Chilean
1501 0001 funded by CONICYT, to the Center for Ad-
intertidal limpets to sea stars. Marine Biology 137, 887–892.
vanced Studies in Ecology & Biodiversity (CASEB) Pro- Fariña, J., Castilla, J.C., 2001. Temporal variation in the diversity and
gram 7. Additional support provided by ICA to JAC is cover of sessile species in rocky intertidal communities affected by
also appreciated. We deeply thank the tireless assistance copper mine tailing in northern Chile. Marine Pollution Bulletin
of C. Camus, P. Villanueva, C. Henrı́quez, C. Lopez, A. 42, 554–568.
Grout, J., Levings, C., 2001. Effects of acid mine drainage from an
Mann, A. Meynard, B. Morandi, V. Oppliger, M. Ra-
abandoned copper mine, Britannia mines, Howe Sound, BC, on
mı́rez and Dr. E. Martı́nez during the extensive and transplanted blue mussels (Mytilus edulis). Marine Environmental
extenuating fieldwork involved in the present study. Research 51, 265–288.
The comments of the anonymous reviewers are appreci- Hunter, M., Price, P., 1992. Playing chutes and ladders: heterogeneity
ated. We deeply thank Paula Neill for significantly and the relative roles of bottom-up and top-down forces in natural
communities. Ecology 73, 724–732.
improving the grammar in the final version of the
Jaccard, P., 1901. Distribution de la flore alpine dans le basin des
manuscript. dranses et dans quelquesregions voisines. Bulletin de la Societe
Vaudoise de Sciences Naturelles 37, 241–272.
Jones, C., Lawton, J., Shachak, M., 1994. Organisms as ecosystem
engineers. Oikos 69, 373–386.
References Kinnear, P., Gray, C., 2000. SPSS for Windows made simple. Release
10. Psychology Press, East Sussex, UK.
Bryan, N., Langston, W., 1992. Bioavailability, accumulation and Krebs, C., 1972. Ecology: The Experimental Analysis of Distribution
effects of heavy metals in sediments with special reference to United and Abundance. Times Printers Sdn. Bhd., Singapore, p. 694.
Kingdom estuaries: A review. Environmental Pollution 76, 89–131. Lancelotti, D., Stotz, W., 2004. Effects of shoreline discharge of iron
Castilla, J.C., 1983. Environmental impacts in sandy beaches of copper mine tailings on a marine soft-bottom community in northern
mine tailing at Chañaral, Chile. Marine Pollution Bulletin 14, 159– Chile. Marine Pollution Bulletin 48, 303–312.
464. Lee, M., Correa, J.A., 2004. Effects of copper mine tailings disposal on
Castilla, J.C., 1988. Earthquake-caused coastal uplift and its effects on littoral meiofaunal assemblages in the Atacama region of northern
rocky intertidal kelp communities. Science 242, 440–443. Chile. Marine Environmental Research 59, 1–18.
Castilla, J.C., 1996. Copper mine tailing disposals in northern Chile Lee, M., Correa, J.A., Zhang, H., 2002. Effective metal concentrations
rocky shores: Enteromorpha compressa (Chlorophyta) as a sentinel in porewater and seawater labile metal concentrations associated
species. Environmental Monitoring and Assessment 40, 171–184. with copper mine tailings disposal into the coastal waters of the
 M. Medina et al. / Marine Pollution Bulletin 50 (2005) 396–409 409

Atacama region of northern Chile. Marine Pollution Bulletin 44, Santelices, B., Ojeda, P., 1984. Recruitment, growth and survival of
956–976. Lessonia nigrescens (Phaeophyta) at various tidal levels in exposed
Lewis, A., 1995. Copper in Water and Aquatic Environments. habitats of central Chile. Marine Ecology Progress Series 19, 73–82.
International Copper Association, Ltd., New York, USA, p. 65. Sneath, P., 1957. Some thoughts on bacterial classification. Journal of
Mardsen, A., DeWreede, R., 2000. Marine macroalgal community, General Microbiology 17, 184–200.
structure, metal content and reproductive function near an acid Stauber, J., Benning, R., Hales, L., Eriksen, R., Nowak, B., 2001.
mine outflow. Environmental Pollution 110, 431–440. Copper bioavailability and amelioration of toxicity in Macquarie
Mardsen, A., DeWreede, R., Levings, C., 2003. Survivorship and Harbour, Tasmania, Australia. Marine Freshwater Research 51, 1–
growth of Fucus gardneri after transplant to an acid mine drainage- 10.
polluted area. Marine Pollution Bulletin 46, 65–73. Tokeshi, M., Estrella, C., Paredes, C., 1989. Feeding ecology of a size-
Metrohm, 2000. Determination of zinc, cadmium, lead and copper by structured predator population, the South American sun-star
anodic stripping voltametry using carbon electrodes. Application Heliaster helianthus. Marine Biology 100, 495–505.
bulletin. No. 254/1 e. Metrohom Ltd., Herisau, Switzerland. Torres, J., 2003. Copper, Environment and human health. Chilean
Paskoff, R., Petiot, R., 1990. Coastal progradation as a by-product of copper commission. Technical advisory committee on copper on
human activity: an example from Chañaral Bay, Atacama Desert, drinking water, Chile, p. 81.
Chile. Journal of Coastal Research 6, 91–102. Vásquez, J., Santelices, B., 1984. Comunidades de macro-invertebra-
Ramı́rez, M., Massolo, S., Frache, R., Correa, J.A. Metal speciation dos en discos adhesivos de Lessonia nigrescens Bory (Phaeophyta)
and environmental impact in sandy beaches due to mine activities en Chile central. Revista Chilena de Historia Natural 57, 131–154.
of El Salvador copper mine, Chile. Marine Pollution Bulletin, in Vásquez, J., Vega, M., Matsuhiro, B., Urzúa, C., 1999. The ecological
press. effects of mining discharges on subtidal habitats dominated by
Ratkevicius, N., Correa, J.A., Moenne, A., 2003. Copper accumula- macroalgae in northern Chile: population and community level
tion, synthesis of ascorbate and activation of ascorbate peroxidase studies. Hydrobiologia 398/399, 217–229.
in Enteromorpha compressa (L.) Grev. (Chlorophyta) from heavy Vermeer, K., Castilla, J.C., 1991. High cadmium residues observed
metal-enriched environments in northern Chile. Plant, Cell and during a pilot study in shorebirds and their prey downstream from
Environment 26, 1599–1608. El Salvador Copper Mine, Chile. Bulletin of Environmental
Riquelme, C., Rojas, A., Flores, V., Correa, J.A., 1997. Epiphytic Contamination and Toxicology 46, 242–248.
bacteria in a copper-enriched environment in northern Chile. Zar, J., 1999. Biostatistical Analysis, fourth ed. Prentice-Hall, Engle-
Marine Pollution Bulletin 34, 816–820. wood Cliffs, NJ, UK, p. 123.