Marine Pollution Bulletin 77 (2013) 71–81

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Marine Pollution Bulletin

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Trace metal enrichments in nearshore sediments and accumulation

in mussels (Modiolus capax) along the eastern coast of Baja California,
Mexico: Environmental status in 1995
Albino Muñoz-Barbosa, Miguel Angel Huerta-Diaz ⇑
Instituto de Investigaciones Oceanológicas, Universidad Autónoma de Baja California, Punta Morro Campus, Kilómetro 103, Carretera Tijuana-Ensenada, Ensenada,
Baja California, Mexico

a r t i c l e i n f o a b s t r a c t

Keywords: The biogeochemistry of trace metals in nearshore sediments and mussel was studied at 15 stations along
Trace metals a 1000 km long transect paralleling the west coast of the Gulf of California (GOC). Total trace metal (Me)
Mussel and enrichment factor (EFMe) values in sediments were low due to negligible anthropogenic influence in
Sediment the region. Past copper mining, however, near Santa Rosalia caused concentrations of Pb, Mn, Co, Zn and
Metal enrichment
Cu which were 10–3.3  103 times greater than the average for the rest of the transect. Mussels also
Gulf of California
showed relatively high trace metal concentrations at the Santa Rosalia stations, but the variability in
the spatial distribution was low and had undefined trends. Our results show that, with the exception
of Co and Cu, the contamination caused by the copper mine affected sediments to a greater extent than
mussels.
Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction southern region (due to tropical storms and hurricanes; Byrne

and Emery, 1960; Lluch-Cota et al., 2007).
The Gulf of California (GOC) is a highly productive (>1 g-C m2 The GOC has one of the most diverse marine biological commu-
d , although it can exceed 4 g-C m2 d-1; Alvarez-Borrego and
1
nities in the world, with 4852 invertebrates species (excluding
Lara-Lara, 1991; Santamaria-del-Angel et al., 1994) marine ecosys- copepods and ostracods), 891 fish species, 222 tetrapods species
tem which supports one of the most important fisheries in Mexico. (Lluch-Cota et al., 2007), as well as at least two endangered species
The GOC presents dry, cold winters, and hot, humid summers, with endemic to the GOC (Bobadilla et al., 2011) that include vaquita
strong winds from the northwest originating from the subtropical porpoise (Phocoena sinus) and the totoaba (Totoaba macdonaldi).
high pressure system of the Eastern Pacific (November through Therefore, it is important to understand the trace element geo-
April). The Northwest winds are responsible for the coastal upwell- chemistry and the potential sources of natural and anthropogenic
ing which occurs along the GOC, specifically in the central and influences in the GOC. Results obtained from this work could prove
southern regions (Douglas et al., 2007). useful in studying other semi-enclosed basins such as the Mediter-
In the northern part of the GOC, which is relatively shallow ranean (e.g., Belabed et al., 2013), Red Sea (e.g., Usman et al., 2013),
(200 m), large quantities of fine grained sediment are resuspended or the Persian Gulf (e.g., Abdollahi et al., 2013; Heidari et al., 2013).
by the strong currents produced by a large tidal range (as high as It is still possible to regard the west coast of the GOC as a pristine
6.95 m in San Felipe; Lluch-Cota et al., 2007). In general, the north- region since there is only one city on the entire west coast of GOC
ern region is dominated by fine grained sediments, however, coar- (La Paz, Baja California Sur, on the southern tip, with approxi-
ser grained sediments are found in all coastal regions. Currently, mately 215,000 inhabitants). In contrast, the east coast of the Gulf
organic production in the water column is the primary source of is contaminated by point sources such as industrial processes (e.g.,
sediments (Byrne and Emery, 1960; Simoneit et al., 1986). The Morales-Hernández et al., 2004), agricultural activities (e.g., Green-
shores of the Baja California Peninsula (BCP) also receive occasional Ruiz and Páez-Osuna, 2001), sewage discharges (e.g., Morales-Her-
fluvial sediment deposition from seasonal rivers and creeks. Fluvial nández et al., 2004), and aquacultural activities (e.g., Páez-Osuna
inputs typically occur during winter storms in the northern region and Ruiz-Fernández, 2005), especially in the state of Sinaloa coasts
of the GOC, and during the summer and part of the fall in the (e.g., Frías-Espericueta et al., 2004; Ruelas-Inzunza et al., 2012)
and, to a lesser extent, in the state of Sonora (e.g., Jara-Marini
⇑ Corresponding author. Tel.: +52 (646) 174 401x167; fax: +52 (646) 174 5303. and García-Rico, 2006). The west coast, however, only has a few
E-mail address: [email protected] (M.A. Huerta-Diaz). population centers with essentially no industrial activity. The only

0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.marpolbul.2013.10.030
72 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81

exception is the town of Santa Rosalia, where there is relatively was dried at room temperature in a laminar flow hood. Herein,
intense anthropogenic impact due to mining by the El Boleo Min- all metals associated to sediments and mussels will be referred
ing Complex (EBMC); founded in 1885 to mine copper carbonate to as trace metals, independently of their concentration.
(Romero Gil, 1991). The mineral extracted from EBMC was up to
20% Cu by weight and, until the end of the nineteenth century, 2.1. Study area and sample collection
represented 50% of the Mexican national copper production
(approximately 11 million tons of pure Cu; Romero Gil, 1991). Organisms and sediment were collected between 14 and 28
The mining district was closed in 1984 but was recently reopened September 1995 at 15 stations along the GOC west coast (Fig. 1).
as part of a joint venture between Canadian and Korean mining The transect on which they were collected was approximately
companies for the production of Cu, Co, Zn and, possibly, Mn. 1000 km in length, from La Paz Bay (Baja California Sur) to Punta
Total trace metal concentrations were measured in superficial Estrella (Baja California). Sample locations were selected due to
sediments and Modiolus capax mussels in order to study their their proximity to population centers on the west coast of the
biogeochemistry, as well as to distinguish potential natural and BCP. In each station superficial sediments and mussels were col-
anthropogenic sources of trace metals along the pristine western lected by a diver; however, mussels were only found in 12 of the
coast of the GOC. Another objective of this work is to establish ref- 15 stations (Table 1). All sediment samples were brown to red in
erence frames for future research. In 1995 sediment samples and color with no hydrogen sulfide smell. Additionally, six (terrestrial)
mussels were collected (Fig. 1) from La Paz Bay (Baja California samples were collected: three from abandoned piles of discarded
Sur) to Punta Estrella (Baja California). Sediment enrichment fac- mine materials (herein referred to as waste) not far from the smel-
tors and geoaccumulation indexes (Igeo; Müller, 1979; Ghrefat ter, and another three samples from an old waste storage tower lo-
et al., 2011) were calculated to assess the magnitude of natural cated in the port of Santa Rosalia. Forty-five mussels (Modiolus
and anthropogenic trace metal sources; these values were then capax) of similar size (8–10 cm) were also collected in each station
compared to trace metal concentrations in mussels to establish in order to avoid variability in metal contents due to size differ-
the type of mechanisms involved in their bioaccumulation. Finally, ences (Boyden, 1977; Latouche and Mix, 1982; Ghrefat et al.,
to evaluate possible consequences to the local biota, trace metal 2011). Furthermore, mussels were also collected from the same
concentrations found in this study were compared with previously tide level to avoid changes in metal concentrations due to differ-
established quality control guidelines for sediments and mussels. ences in tidal exposure time (Coleman, 1980; Mubiana et al.,
2006). Once collected, the mussels were stored in trace metal-free
polyethylene bags, which were sealed and placed on ice (4 °C) in
2. Materials and methods the field until frozen at 20 °C. Sediments were collected at
variable water depths (3–5 m) with a polycarbonate core (7.2 cm
All laboratory materials were washed with phosphate-free interior diameter) which was used to collect the first 3–4 cm of
detergent, rinsed three times with distilled water and the soaked the sediment. Each sample represents the mixing of three subsam-
in a 5% HCl solution for 24 h. After the acid bath the material ples collected at each site that were mixed in the field. Sediment
was rinsed three times with Milli-Q grade deionized water and samples were stored in acid-clean plastic bags and preserved on

Fig. 1. Study area and location of the 15 sampling sites of sediments and mussels. Squares represent stations where only sediments were collected.
 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81 73

Table 1
Stations where samples of sediments and mussels (Modiolus capax) were collected with their corresponding location, station codes, collection dates and percentages of grain size
<62.5 lm.

No. Station Code Location Collection date Superficial Mussel Grain size
sediment <62.5 lm (%)
Latitude (N) Longitude (W)
1 La Paz, Baja California Sur (BCS) LPZ 24°10.2770 110°18.5190 14-September-1995 YES NO 24.3
2 Loreto, BCS LTO 25°55.7160 111°21.2120 15-September-1995 YES NO 11.7
3 Mulegé, BCS MGE 26°53.9530 111°57.1750 16-September-1995 YES YES 9.5
4 Estero San Lucas 1, BCS ESL1 27°12.4400 112°12.0690 17-September-1995 YES NO 48.0
5 Estero San Lucas 2, BCS ESL2 27°14.2410 112°11.5060 17-September-1995 YES YES 6.8
6 Santa Rosalia North, BCS SRN 27°23.3830 112°18.2330 18-September-1995 YES YES 21.4
7 Santa Rosalia South, BCS SRS 27°19.5260 112°14.5680 18-September-1995 YES YES 9.9
8 El Barril, Baja California (BC) EBR 28°18.4170 112°52.4740 20-September-1995 YES YES 4.1
9 San Francisquito, BC SFC 28°24.4150 112°51.4760 20-September-1995 YES YES 7.3
10 Bahía de los Angeles (Rincón), BC BAR 28°53.4760 113°29.9720 23-September-1995 YES YES 7.6
11 Bahía de los Angeles (Centro), BC BAC 28°58.3240 113°32.6900 23-September-1995 YES YES 10.3
12 Bahía de los Angeles (Gringa), BC BAG 29°02.3650 113°32.7040 24-September-1995 YES YES 10.1
13 Bahía de San Luis Gonzaga, BC BSL 29°47.6450 114°23.7440 26-September-1995 YES YES 29.6
14 Puertecitos, BC PRT 30°22.0530 114°38.4320 27-September-1995 YES YES 10.9
15 Punta Estrella, BC PES 30°56.2310 114°43.2430 28-September-1995 YES YES 8.6

Table 2
Percent recovery calculated from measured and certified values (± one standard deviation) of the reference materials (CRM’s) BCSS-1 (marine sediment, National Research
Council, Canada) and 1566a (oyster tissue, National Institute of Standards and Technology, USA) for sediments and mussels, respectively. Precision of the analysis (square
brackets) is expressed as the percentage of the relative standard deviation of the corresponding measured value. Average total trace metal concentrations (± one standard
deviation) for all stations calculated with and without Santa Rosalía (SR) stations. The asterisks indicate values that could not be calculated because the concentrations of the
CRM’s were below their corresponding detection levels.

Element Measured value (lg g1) Certified Recovery Detection Average total trace Average total trace metal
value (lg g1) percentage limit (lg g1) metal (lg g1) without SR (lg g1)
Sediments
Al (6.58 ± 0.16)  104 [2.5] (6.260 ± 0.216)  104 105 54 – –
Cd 0.27 ± 0.01 [3.3] 0.25 ± 0.10 108 0.033 43 ± 34 46 ± 34
Co 11.1 ± 0.2 [1.9] 11.4 ± 2.1 97 1.5 2.0 ± 1.2 1.7 ± 1.2
Cu 19.4 ± 0.1 [0.72] 18.5 ± 2.7 105 1.1 22 ± 14 17 ± 14
Fe (3.18 ± 0.06)  104 [2.4] (3.29 ± 0.10)  104 97 12 (2.4 ± 2.0)  102 (2.5 ± 2.0)  102
Mn 221 ± 2 [0.76] 229 ± 15 97 2.1 (3.8 ± 4.4)  102 (3.8 ± 4.4)  102
Ni 54 ± 4 [7.3] 55.3 ± 3.6 102 3.3 4.6 ± 2.8 5.0 ± 2.8
Pb 20.9 ± 0.4 [2.4] 22.8 ± 3.3 92 3.7 2.7 ± 2.9 2.7 ± 2.9
Zn 116.1 ± 0.1 [0.85] 119 ± 12 98 0.85 129 ± 51 125 ± 51
Mussels
Cd 3.86 ± 0.16 [4.1] 4.15 ± 0.38 93 0.11 43 ± 28 46 ± 30
Co 0.14 ± 0.20 [⁄] 0.57 ± 0.11 ⁄
0.31 1.9 ± 1.2 1.7 ± 1.1
Cu 58.7 ± 2.3 [3.9] 66.3 ± 4.3 89 0.11 21 ± 12 17.2 ± 7.0
Fe 485 ± 28 [5.9] 539 ± 15 90 0.45 235 ± 168 246 ± 184
Mn 11.2 ± 1.2 [10] 12.3 ± 1.5 91 0.24 379 ± 401 379 ± 445
Ni 2.41 ± 0.76 [32] 2.25 ± 0.44 108 0.65 4.7 ± 2.7 5.0 ± 2.9
⁄
Pb 0.352 ± 0.041 [12] 0.371 ± 0.014 0.91 2.7 ± 2.9 2.7 ± 3.1
Zn 922 ± 242 [26] 830 ± 569 111 0.085 129 ± 47 125 ± 51

ice (4 °C) until frozen at 20 °C. Sediments and organisms were material (CRM) SRM-1566a (oyster tissue; National Institute of
collected as close together as possible; mussels were not Standards and Technology) were analyzed. The recovery percent-
depurated. ages from the CRM’s (Table 2) were between 89% (Cu) and 111%
Organisms were defrosted and dissected, rinsed with deionized (Zn). The percent of water in the tissues samples as well as the per-
water, and then separated into three subsamples which were a cent of dry mussel tissue were calculated by drying approximately
composite of 15 mussels. Dissected tissue was individually 5.0 g of wet sample at 70 °C during 72 h (weighing the sample be-
weighted and placed in clean plastic vials. The tissue from each fore and after drying). All mussel concentrations are reported on
replicate was homogenized with a Virtis Titanium-Blade homoge- the basis of dry weight (dw), except when comparisons with guide-
nizer, an aliquot of 5 g was placed into 25 ml glass beakers and lines for human consumption are made, in which case the relevant
5 ml of concentrated HNO3 (trace metal grade) were added to the concentrations will be properly identified and discussed using wet
samples. The beakers were covered with a watch glass and left to weights (ww), as is normally reported in the literature.
react overnight at room temperature. In the morning, the samples Total sediment digestions were carried out according to the
were placed on a heating plate at 50 °C for 2 h, digested under re- method described by Carignan and Tessier (1988). Briefly, this
flux at 100 °C over 4 h and then evaporated to until they were dry. method involves the digestion of 0.5 g dry weight of sample (dried
Finally, samples were redissolved with 20 ml of 1% HNO3 (v/v) and at 80 °C in an oven until constant weight was obtained) which is
transferred to 30 ml polypropylene vials. To confirm the accuracy sequentially digested with 15 ml of concentrated HNO3, 4 ml of
and precision of the analytical procedures, for each 15 samples concentrated HClO4, and 10 ml of concentrated HF. Finally, after re-
one procedural blank and one sample of certified reference flux, samples were redissolved in 5% HCl bringing the volume up to
74 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81

" #
50 ml. The final solution was always clear with no visible residues. ðMe=AlÞsample
The CRM BCSS-1 (marine sediment; National Research Council, EFMe ¼ ð1Þ
ðMe=AlÞclay
Canada) was used to confirm the accuracy and precision of the ana-
lytical procedures, with recovery percentages (Table 2) covering a where the subscripts sample and clay refer to the Al-normalized
range of 92% (Pb) to 108% (Cd). The percentage of the <62.5 lm values of the sample and avcsr, respectively. If EFMe > 1 the metal
grain size fraction (clay and silt) in the sediment samples was concentration in the sample is enriched relative to the average
determined by the pipette method of Folk (1968). value in the Earth’s crust and, therefore, anthropogenically, biolog-
Total trace metal (Me) concentrations in mussel tissues (Cd, Co, ically, or diagenetically enriched. If EFMe < 1 the metal is impover-
Cu, Fe, Mn, Ni, Pb, Zn) and sediments (the aforementioned metals ished relative to avcsr, possibly due to diagenetic processes that
as well as Al) were measured with a Thermo Jarrel Ash model reduced the metal concentration of the sample; and finally, if
Smith Hieftje graphite furnace atomic absorption spectrophotome- EFMe = 1 the metal concentration is neither enriched nor
ter. Trace metal detection limits for sediments and mussel tissues impoverished.
were calculated as three times the standard deviation of the proce- We also calculated the geoaccumulation index (Igeo), introduced
dural blank (Table 2). by Müller (1979), which is a unitless quantitative measurement of
trace metal contamination in sediments. It is an intensity
2.2. Data treatment classification consisting of seven classes: <0 = unpolluted (UP),
0–1 = unpolluted to moderately polluted (UP–MP), 1–2 = MP,
Trace metal enrichment factors (EFMe) in sediments were calcu- 2–3 = MP to strongly polluted (MP–SP), 3–4 = SP, 4–5 = SP to very
lated by normalizing trace metals concentrations (Me) to Al (a con- strongly polluted (SP–VSP), and > 5 = VSP; with the maximum level
servative element). For the EFMe calculation, it is recommended to reflecting at least an enrichment 100 times above an established
use local background values. In this case such information is not baseline. The Igeo is calculated with the equation (Müller, 1979):
available for the study region; therefore, Earth’s average values of  
ðMeÞsample
clays from sedimentary rocks (avcsr) reported by Turekian and Igeo ¼ log2 ð2Þ
1:5ðMeÞbaseline
Wedepohl (1961) and Li and Schoonmaker (2005) were used
instead. The EFMe values were calculated using the following where (Me)baseline represents avcsr (taken from Turekian and Wed-
equation: epohl, 1961 and Li and Schoonmaker, 2005), and 1.5 is a constant

Fig. 2. Average total concentrations of Cd, Co, Cu, Fe, Mn, Ni, Pb, and Zn in sediments for all the sampling sites included in this study (dashed lines indicate Santa Rosalia). Data
from La Paz (Shumilin et al., 2001), Santa Rosalia (Shumilin et al., 2000), Bahia de San Luis Gonzaga, Puertecitos, and Punta Estrella (Daesslé et al., 2002) are included for
comparative purposes. For the specific case of Santa Rosalia the values reported by Shumilin et al. (2000) are from nearby creeks, mine wastes, sand beaches, and coastal
sediments. See Table 1 for station codes equivalence. Error bars for the samples collected in this study represent the standard deviation of laboratory replicates, except the
ESL, SR and BA values, which correspond to the means of stations ESL1 and ESL2, SRN and SRS and BAR, BAC, and BAG, respectively.
 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81 75

included due to possible variations in the background value pro- SigmaStat 3.5 software package. If the normality test failed, then
duced by lithogenic effects (Salomons and Förstner, 1984). a Mann–Whitney Rank Sum test was applied.
The possible biological consequences arising from the trace
metal concentrations measured in each of the sampling stations
were evaluated using the classification of Long et al. (1995). This 3. Results and discussion
classification system establishes quality control guidelines which
identify potential effects range-low (ERL: 10% of the Long et al., 3.1. Total trace metal concentrations in sediments
1995 data falls within this range) and effects range-median
(ERM: the median or 50th percentile of the data is represented in Average total metal concentrations follow the order Cd < Pb 
this range) adverse effects. Therefore, values which are <ERL Co < Ni  Cu < Zn < Mn < Fe (not including sites samples from San-
represent metal contamination where biological effects are rarely ta Rosalia due to their extremely high values, see methods). Total
observed, values between ERL and ERM will have occasionally metal concentrations at the remaining sites were relatively low
observed biological effects, and concentrations >ERM represent in comparison to other regions around the world due to the high
values where biological effects will be frequently present. Mussel content of sand (52–96%; Table 1). The dilution effect of sand is
trace metal concentration ranges established by NOAA were used more evident when comparing this study’s concentrations with
to evaluate relative differences between zones (Kimbrough et al., values from sediments with finer grain size. For example, if we
2008). These ranges were determined using data from the years compare our values without the Santa Rosalia samples (MeGDC)
2004 and 2005 obtained from mussels and oysters collected from with those reported for sediments from the Baja California Pacific
various coastal zone regions of the United States. Concentrations coast (MePAC; Nava-López, 2002), the following MeGDC/MePAC
that were used to determine the low, medium, and high ranges values are obtained: 0.0064, 0.051, 0.063, 0.071, 0.40, 0.77, 0.89
were calculated using cluster analysis. It should be noted that this and 9.2 for Fe, Pb, Co, Ni, Cu, Mn, Zn and Cd, respectively. The
classification system is not used to represent concentrations or Pacific coast of Baja California is generally regarded as a relatively
levels associated to public health risks. Whenever two sets of data pristine region (Villaescusa-Celaya et al., 2000), except in areas
were compared, Student’s t-tests were carried out using the very close to wastewater outfalls (specifically the Punta Bandera

Fig. 3. Enrichment factors (EFMe) and average mussel concentrations (± one standard deviation) of Cd, Co, Cu, Fe, Mn, Ni, Pb and Zn for all the different sampling sites included
in this study. Locations 1–15: sampling sites from this study (see Table 1 for station codes equivalence). Location 16: average of 50 samples (no standard deviation reported)
collected near Guaymas Harbor, Gulf of California (Brumsack, 1989). Locations 17 and 18: average (± one standard deviation) EFMe with and without considering the SR
values, respectively. Locations 19 and 20: average (± one standard deviation) mussel concentrations with and without considering the SR values, respectively. The horizontal
dashed lines indicate the value when EFMe = 1. Values above or below this line correspond to enrichments or impoverishments of metals in sediments, respectively. The
shadowed area corresponds to the Santa Rosalia (SR) sampling sites. Note that no mussels were collected in La Paz (LPZ), Loreto (LTO) and Estero San Lucas 1 (ESL1). Dotted
gray lines indicate missing data.
76 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81

outfall, close to the city of Tijuana). Trace metal enrichments along

Baja California are generally associated with physical oceano-
graphic processes such as upwelling and advection, rather than
with anthropogenic inputs (Sañudo-Wilhelmy and Flegal, 1991).
The MeGDC/MePAC values show that metal concentrations in coarse
grained sediments of the western coast of GOC are lower than
those measured in fine grained sediments of the Pacific coast of
Baja California. The only exception was Cd, which had a mean total
concentration nine times higher than that measured in samples
from the Pacific coast of Baja California.
A common feature of the GOC in this and other studies (e.g.,
Shumilin et al., 2000; Cadena-Cárdenas et al., 2009), are the extre-
mely high concentrations of Co, Cu, Pb and Zn found in sediments
of the Santa Rosalia area (Fig. 2). If values from this location are not
considered (areas enclosed by the dashed lines in Fig. 2), total con-
centrations of Cd, Co, Cu, Zn, and to a certain extent Pb, show rel-
atively low concentrations and variability. As it will be shown
herein, the high concentrations measured in Santa Rosalia are
not due to natural biogeochemical processes, but rather to waste
and slag that was produced by the old EBMC. In contrast, our re-
sults indicate that concentrations of Cd, Fe, and Ni were not influ-
enced by EBMC. Fig. 2 shows that in general, there was agreement
between the concentrations measured in this study and those re-
ported in the literature. Concentrations of Fe and Mn decrease from
La Paz to Santa Rosalia and then increase from Santa Rosalia to
Punta Estrella (Fig. 2).

3.2. Enrichment factors and geoaccumulation index

3.2.1. Cadmium enrichment

Enrichment factors (EFMe) determine whether the variability in
total metal concentrations are the result of natural mineralogical
Fig. 4. (a) Geoaccumulation indexes (Igeo; Müller, 1979) of Al, Cd, Co, Cu, Fe, Mn, Ni, variability, anthropogenic induced changes, and/or grain size
Pb and Zn for all the different sampling sites included in this study (sampling site distribution. EFMe spatial distributions (Fig. 3) show that all metals,
codes as shown in Table 1). The intensity classification of Igeo consist of seven except Cd, are near or below their corresponding avcsr. Cadmium
classes: under polluted = <0 (UP), under polluted to moderately polluted = 0–1 (UP–
MP), moderately polluted = 1–2 (MP), moderately to strongly polluted = 2–3 (MP–
was the only element whose enrichment was consistently high at
SP), strongly polluted = 3–4 (SP), strongly to very strongly polluted = 4–5 (SP–VSP) all stations, with values ranging from 8.7 to 32 and with averages
and very strongly polluted = >5 (VSP). (b) Average concentrations (± one standard of 16 ± 7 and 16 ± 8 for the entire study zone (with and without the
deviation) of trace metals in mussel tissue vs. average (± one standard deviation) Santa Rosalia stations, respectively; Fig. 3). With the exception of
sediment enrichment factors (EFMe). Data from Santa Rosalia was not included (see
EBMC in Santa Rosalia, industry was practically non-existent and
text for explanation). The vertical dashed gray line represents the value when
EFMe = 1. Note the log scale in both axes. human settlements were spatially far apart and relatively small
in size in the GOC. Therefore, a relationship between Cd
enrichments and anthropogenic influence is unlikely. Cadmium

Table 3
Average ± one standard deviation (SD) of total trace metal concentrations (Me) and enrichment factors (EFMe) of mine waste and slags from El Boleo Mine, Santa Rosalía, Baja
California Sur. Three samples were collected from abandoned piles of mine waste (Waste) on land and from a waste delivery tower (Tower) located on the pier of the Port of Santa
Rosalía.

Sample Al (lg g1) Cd (lg g1) Co (lg g1) Cu (lg g1) Fe (lg g1) Mn (lg g1) Ni (lg g1) Pb (lg g1) Zn (lg g1)
4 3 4 4
Tower 1 5.86  10 – 1.65  10 – 8.9  10 4.71  10 69 – 5.23  103
Tower 2 6.93  104 11.8  103 1.53  103 3.50  103 8.8  104 4.18  104 67 2.0  102 4.58  103
Tower 3 6.85  104 – 1.67  103 3.24  103 9.4  104 4.15  104 76 1.8  102 4.84  103
Slag 1 6.37  104 – 9.19  103 – 6.6  104 6.32  104 53 – 6.60  103
Slag 2 7.47  104 6.74  103 1.03  103 10.2  103 7.1  104 5.93  104 56 10  102 6.54  103
Slag 3 7.66  104 – 0.972  102 9.98  103 6.9  104 5.88  104 51 8.9  102 6.28  103
Average 6.85  104 9.22  103 1.30  103 6.7  103 7.9  104 5.19  104 62 5.6  102 5.69  103
SD 0.68  104 3.60  103 0.36  103 3.9  103 1.2  104 0.96  104 10 4.4  102 0.92  103
EFCd (mass ratio) EFCo (mass ratio) EFCu (mass ratio) EFFe (mass ratio) EFMn (mass ratio) EFNi (mass ratio) EFPb (mass ratio) EFZn (mass ratio)
Tower 1 – – 1.4  104 – 8.2  105 4.31  105 6.0  102 – 4.08  104
Tower 2 – 4.5  104 1.1  104 2.4  104 6.8  105 3.27  105 4.9  102 0.41  103 3.01  104
Tower 3 – – 1.2  104 2.2  104 7.3  105 3.29  105 5.7  102 0.38  103 3.25  104
Slag 1 – – 0.74  104 – 5.6  105 5.36  105 4.2  102 – 4.77  104
Slag 2 – 2.4  104 0.70  104 6.4  104 5.1  105 4.31  105 3.9  102 1.94  103 4.01  104
Slag 3 – – 0.64  104 6.2  104 4.8  105 4.17  105 3.4  102 1.69  103 3.74  104
Average – 3.5  104 0.98  104 4.3  104 6.3  105 4.12  105 4.7  102 1.11  103 3.81  104
SD – 1.5  104 0.33  104 2.3  104 1.3  105 0.78  105 1.0  102 0.83  103 0.63  104
 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81 77

Table 4
Sediment quality guidelines values of effects range-low (ERL) and effects range-median (ERM) for trace metals (taken from Long et al., 1995) and contamination levels (in lg g1
and lmol g1) for trace metals in mussels established by NOAA (Kimbrough et al., 2008). Included are incidence percentages (and ratios of incidence) of all stations as well as their
classification in each guideline: (a) La Paz, (b) Loreto, (c) Mulegé, (d) Estero San Lucas 1, (e) Estero San Lucas 2, (f) Santa Rosalía South, (g) Santa Rosalia North, (h) El Barril, (i) San
Francisquito, (j) Bahía de los Angeles Rincon, (k) Bahía de los Angeles Centro, (l) Bahía de los Angeles Gringa, (m) San Luis Gonzaga, (n) Puertecitos, and (o) Punta Estrella. For
sediments Long et al. (1995) calculated the ERL and ERM values only for Cd, Cu, Ni, Pb, and Zn, whereas for mussels Kimbrough et al. (2008) calculated the values only for Cd, Cu,
Ni, Pb, and Zn.

Element ERL guideline (lg g1) ERM guideline (lg g1) Percentage (ratio) of incidence Station classification
<ERL ERL–ERM >ERM <ERL ERL–ERM >ERM
Sediments
Cd 4.9 40 87 (13/15) 13 (2/15) 0 (0/15) a, b, c, e, g, h, i, j, k, l, m, n, o d, f –
Cu 34 270 80 (12/15) 13 (2/15) 7 (1/15) a, c, d, e, h, i, j, k, l, m, n, o b, g f
Ni 20.9 51.6 80 (12/15) 13 (2/15) 7 (1/15) a, b, d, e, h, i, j, k, l, m, n, o c, g f
Pb 46.6 218 93 (14/15) 7 (1/15) 0 (0/15) a, b, c, d, e, g, h, i, j, k, l, m, n, o f –
Zn 150 410 87 (13/15) 7 (1/15) 7 (1/15) a, b, c, d, e, h, i, j, k, l, m, n, o g f
Element Low level Medium level High level Percentage (ratios) of incidence Station classification
(lg g1) (lg g1) (lg g1)
Low level Medium level High level Low Medium High
Mussels
Cd 0–3 4–9 10–20 0 (0/12) 8 (1/12) 92 (11/12) – o c, d, f, g, h, i, j, k, l, m, n
Cu 5–16 17–39 40–857 42 (5/12) 50 (6/12) 8 (1/12) c, h, j, k, l d, g, i, m, n, o f
Ni 0–5 6–14 15–44 75 (9/12) 25 (3/12) 0 (0/12) f, g, h, i, j, k, l, m, o c, d, n –
Pb 0–3 4–6 7–13 84 (10/12) 8 (1/12) 8 (1/12) c, d, f, g, h, i, j, k, l, m o n
Zn 48–139 140–320 321–11,500 50 (6/12) 33 (4/12) 17 (2/12) h, i, j, k, l, m c, d, f, g n, o

enrichments due to contributions from phosphorites are likely Harbor (Romero Gil, 1991), and was also discarded along the coast.
(e.g., the San Gregorio Formation; Piper, 1991), but they are local- Mine slag analysis (Table 3) showed extremely high metal concen-
ized and would produce enrichments in only a few of the southern trations (from as low as 51 lg g1 for Ni to 9.4  104 lg g1 for Fe),
stations. High EFCd values in the GOC (16 ± 7) are similar to enrich- which resulted in enrichment factors ranging from 3.4  102 to
ment values (EFCd = 14) based on trace metal data reported by 8.2  105 for Ni and Fe, respectively (Table 3).
Brumsack (1989) for sediments collected near Guaymas Harbor. Despite the EFCd and Igeo results, it is important to note that
High EFCd have also been reported for the Mexican Pacific (21 ± 9, according to the NOAA Sediment Quality Guide (SQG), developed
or approximately 24% higher than in the GOC; Nava-López, by Long et al. (1995), in 13 of the 15 studied stations (87%) Cd con-
2002), indicating that Cd is the only element significantly enriched centrations indicate that potential adverse effects on biota should
in these two regions. The San Clemente and Santa Catalina basins be rarely observed (Table 4). Furthermore, only Cd concentrations
in Southern California (EFCd = 3.0 ± 0.7; Bertine and Goldberg, in sediments from Estero San Lucas 1 and Santa Rosalia South are
1977), the northwest US margin (EFCd = 1.9 ± 1.2; Morford and classified as having occasional adverse effects (Table 4). According
Emerson, 1999), and the Virginian and Louisianian provinces to this classification, between 80% and 93% of the concentrations of
(EFCd = 3.3 ± 0.3 and 1.30 ± 0.07, respectively; Weisberg et al., Cd, Cu, Ni, Pb, and Zn are below values which are known to produce
2000), however, do not exhibit high Cd enrichments. Therefore, low-range effects (<ERL) and, therefore, are classified as having
we hypothesize that Cd enrichment in sediments may be unique minimum adverse effects on biota (Long et al., 1995). Only Cu,
to this region and would require further investigations. Ni, and Zn concentrations in Santa Rosalia South were classified
The origin of such high Cd enrichments is due to the biogeo- as producing occasional adverse effects (>ERM; Table 4).
chemical cycle of Cd in the oceans, which is closely tied to organic
matter. The spatial distribution of dissolved Cd is controlled by 3.3. Metal concentrations in mussels
phytoplankton uptake in surface waters which transfer this ele-
ment to underlying sediments via sinking of organic particulates According to Fig. 3, unlike the other metals, Co and Cu have rel-
(Byrne and Emery, 1960). Finally, our findings of natural Cd enrich- atively high values in SRS. The highest Co concentration, however,
ment are also evident in our high geoaccumulation index values is observed in PRT, similar to Mn, Ni, Pb, and Zn. Manganese, Ni,
(Igeo, Müller, 1979): sediments in the study area are moderately and Pb showed maximum values in the northern portion of the
to strongly contaminated, with Cd values in the range 2 < Igeo < 4 study area, with 1.4  103, 11, and 10 lg g1 dry weight (dw),
at all locations (Fig. 4a). respectively, whereas the maximum Fe concentration was in the
southern region (7.0  102 lg g1) and the Cd maximum was more
3.2.2. EFMe Santa Rosalia anomaly towards the central region (1.1 lg g1). Unlike our average results
High trace metal concentrations found in Santa Rosalia North for sediment enrichment factors, average concentrations in
and South (SRN and SRS, respectively) produced elevated average mussels (with and without the Santa Rosalia values) showed no
enrichment factors of Co, Cu, Mn, Zn and, to a certain extent, Pb significant differences amongst themselves (p 6 0.05). These
(Fig. 3). Sediments from most of the other locations show no results suggest, with the exception of Co and Cu (Fig. 3), that the
enrichment and in some cases they are impoverished (EFMe < 1). pollution caused by the copper mine affected sediments to a great-
The influence of the mine waste and slag from the EBMC is evident er extent than mussels. These differences between sediments and
when comparing the mean enrichment factors of the aforemen- mussels could be the result of metal fractionation: total metal
tioned five trace elements with and without considering the sta- analyses quantify both the non-bioavailable and bioavailable frac-
tions from Santa Rosalia (2.9 vs. 0.33, 128 vs. 0.34, 2.7 vs. 0.61, tions, whereas mussels incorporate only the bioavailable fraction
66 vs. 0.50 and 1.3 vs. 0.68, respectively). The EFMe found in Santa of trace metals (excluding their gut contents, which can include
Rosalia, especially those from the southern station, are the result of non-bioavailable particulates).
mine wastes and slag from mining at EBMC. When the mining It would be expected that the higher the metal concentration of
complex was active the slag was used to build the Santa Rosalia a given element in sediments, the higher the concentration that
78 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81

enrichment or sediment impoverishment. Conversely, any value

below the regression line is interpreted as either mussel tissue
impoverishment or sediment enrichment.
Since Cd and Mn showed a high dispersion in relation to the
regression line in Fig. 5a, we considered that these two trace met-
als could be anomalies within the context of the relationship Me/
Al:OrgMe produced by natural and/or anthropogenic factors. Conse-
quently, a second regression (log–log) relationship was calculated
without considering Cd and Mn. This second line showed improve-
ment in the value of the correlation coefficient, from r = 0.68 (n = 8,
p = not significant) when Cd and Mn were included, to r = 0.93
(n = 6, p 6 0.01) when these two metals were not considered
(Fig. 5b). Despite Cd being the only element enriched in sediments,
this enrichment was not reflected in mussel tissue concentrations
(Fig. 4b). On the other hand, it can be also observed in this figure
that, although impoverished in sediments, some elements in the
mussels (e.g., Mn, Fe and Zn) show higher concentrations than
Cd (Fig. 4). These results agree with those reported by Cadena-
Cárdenas et al. (2009), where it was found that enrichments caused
by mining in the GOC were independent of metal concentrations
measured in the mussel Mytilus edulis and the clams Laevicardium
elatum, Megapitaria squalida and Chione californiensis. High concen-
trations of Mn (717–1628 lg g1), Al (635–939 lg g1), and Zn
(219–295 lg g1) in mussels have been reported in the northern
GOC and were attributed to incorporation of sedimentary particu-
late material and/or accumulation mechanisms in the digestive
tract of organisms (Gutiérrez-Galindo et al., 1999). We conclude
that even though trace metals were likely ingested by mussels,
they were not necessarily assimilated (Oullete, 1981; Robinson
et al., 1993).

3.4. Trace element guideline levels in mussels

The levels of the Kimbrough et al. (2008) classification scale

were established on the basis of a statistical classification (hierar-
chical clustering analysis) and are not associated with corrective
measures or human health advisory concentrations. It is, however,
feasible to use this classification to make inferences about our
results concerning contamination levels. Table 4 shows that the
majority of the Cd concentrations measured in the organisms are
high. Organisms at Punta Estrella had medium levels of contamina-
tion, while the rest of the stations (92%) had high levels of contam-
ination. These results could be a consequence of the general Cd
Fig. 5. Average trace metal concentrations (± one standard deviation) in mussel
tissue vs. average mass metal:aluminum (Me/Al) ratios (± one standard deviation)
enrichments found in the GOC. On the other hand, only the organ-
for (a) all metals analyzed, and (b) all metals analyzed except Cd and Mn. The isms collected at Santa Rosalia had high Cu contamination, six
continuous and dashed lines represent the linearization of the data processed in other stations (50%) had medium levels and five (42%) had low
each case and the 95% confidence interval, respectively. Note the log scale in all levels. Thus, due to mining for over 100 years by EBMC, mussels
axes.
found in or near Santa Rosalia (Table 4) have Cu concentrations
that place them in the medium and high contamination levels of
the Kimbrough et al. (2008) classification. Ni was the only metal
metal will be in the tissue of organisms; due to the influence of to not have concentrations which placed it in the high contamina-
that particular sediment. No significant linear correlations tion level category: 75% of stations were classified within the
(p 6 0.05), however, were found between metal concentrations in medium level and only three (25%) were included in the low level
sediments and their corresponding concentrations in organisms. (Table 4). For Pb, 84% of stations were classified in the low contam-
Since metal concentrations in sediments depend on the grain size, ination level, one in the medium (Punta Estrella) and one in the
we present Al-normalized trace metal concentrations in sediments. high (Puertecitos). For Zn, 50% of the stations were classified in
The normalization compensates for the mineralogical and grain the low, 33% in the medium, and 17% in the high contamination
size variability. Fig. 5a shows the result of plotting Al-normalized level categories (the ones located in the northern most portion of
sediment trace metal concentrations (Me/Al) and average mussel the transect; Table 4).
tissue trace element concentrations (OrgMe), where the regression The naturally high concentrations and enrichments of Cd are of
(log–log) line is the ‘‘natural existing relationship’’ between the particular interest because chronic exposures to this element could
above mentioned variables. In other words, trace metals located cause kidney damage (Widmeyer et al., 2004) and osteoporosis in
on or near (field defined by the 95% confidence level dashed lines humans (itai-itai disease; Han et al., 2000). To prevent health risks,
in Fig. 5a) the regression line (continuous line) shown in Fig. 5a national and international organizations have established maxi-
will be close to the ideal relationship Me/Al:OrgMe. Any metal value mum acceptable levels of Cd in seafood. The Mexican standard
above the regression line is interpreted as either mussel tissue NOM-031-SSA1-1993 (NOM, 1995) and the European Union
 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81 79

Table 5
Percentage of water and dry tissue for the mussel samples collected in the different Gulf of California locations.

Location Water (%) Tissue (%) Location Water (%) Tissue (%)
Mulegé 86.2 13.8 Estero San Lucas 2 85.1 14.9
Mulegé 86.9 13.1 Estero San Lucas 2 83.7 16.3
Mulegé 81.0 19.0 Estero San Lucas 2 83.2 16.8
Average 84.7 15.3 Average 84.0 16.0
Standard deviation 3.2 3.2 Standard deviation 1.0 1.0
Santa Rosalía North 81.5 18.5 Santa Rosalía South 80.2 19.8
Santa Rosalía North 82.2 17.8 Santa Rosalía South 80.7 19.3
Santa Rosalía North 81.1 18.9 Santa Rosalía South 80.7 19.3
Average 81.6 18.4 Average 80.5 19.5
Standard deviation 0.6 0.6 Standard deviation 0.3 0.3
El Barril 81.3 18.7 San Francisquito 92.0 8.0
El Barril 82.3 17.7 San Francisquito 79.4 20.6
El Barril 80.6 19.4 San Francisquito 78.5 21.5
Average 81.4 18.6 Average 83.3 16.7
Standard deviation 0.9 0.9 Standard deviation 7.6 7.6
Bahía de los Angeles (Rincón) 76.4 23.6 Bahía de los Angeles (Centro) 82.1 17.9
Bahía de los Angeles (Rincón) 76.0 24.0 Bahía de los Angeles (Centro) 81.3 18.7
Bahía de los Angeles (Rincón) 77.5 22.5 Bahía de los Angeles (Centro) 84.9 15.1
Average 76.6 23.4 Average 82.8 17.2
Standard deviation 0.8 0.8 Standard deviation 1.9 1.9
Bahía de los Angeles (Gringa) 76.1 23.9 Bahía de San Luis Gonzaga 78.1 21.9
Bahía de los Angeles (Gringa) 76.7 23.3 Bahía de San Luis Gonzaga 79.3 20.7
Bahía de los Angeles (Gringa) 76.3 23.7 Bahía de San Luis Gonzaga 77.5 22.5
Average 76.4 23.6 Average 78.3 21.7
Standard deviation 0.3 0.3 Standard deviation 0.9 0.9
Puertecitos 80.0 20.0 Punta Estrella 80.9 19.1
Puertecitos 79.0 21.0 Punta Estrella 81.0 19.0
Puertecitos 82.2 17.8 Punta Estrella 79.3 20.7
Average 80.4 19.6 Average 80.4 19.6
Standard deviation 1.7 1.7 Standard deviation 0.9 0.9

Regulation Commission (EURC, 2008) established a level of Cd than those from the Pacific coast of Baja California (Muñoz-
1.0 mg kg1 wet weight (ww) of Cd (see Table 5 for equivalences Barbosa et al., 2000).
between mussel wet and dry weight), while the US Food and Drug Considering that the information presented in this work was
Administration (FDA, 2003) set a level of 4 mg kg1 ww. The con- based on samples collected well before the opening of the new
centrations found in this study (2.6–15 mg kg1 ww) exceed the Korean–Canadian open-pit mine in Santa Rosalia, our results may
Mexican and European Union limits by a factor of 2–15. Further- serve as a baseline for future evaluations of the impact of the
more, despite the fact that the FDA limit is higher, only one of new mine on the GOC environment.
our 12 stations had concentrations below the 4 mg kg1 ww limit.
The rest of the stations ranged from being slightly above (El Barril
and Estero San Lucas) to exceeding this limit by a factor of 4 (San 4. Conclusions
Francisquito and San Luis Gonzaga).
The Cd Provisional Tolerable Weekly Intake (7 lg kg1 of body Cadmium was the only element consistently enriched in the
weight per week), term used by the FAO/WHO Joint Experts Com- sediments over the study area. This enrichment is a general feature
mittee on Food Additives to determine the amount of a given con- of sediments of the western coast of the GOC (16 ± 7) and the
taminant that a 60 kg adult could consume without representing a Pacific coast of the Baja California peninsula (21 ± 9). Data available
health risk, was estimated at 0.42 mg (FAO/WHO, 2004; Olmedo from other regions of the world indicate that Cd enrichments could
et al., 2013). In other words, if a batch of mussels has a Cd concen- be a particular feature present only in these two regions.
tration of 0.21 mg kg1, a 60 kg adult could eat 2 kg per week of Apparently, the processes producing these enrichments are not
these organisms without a possible health risk. Using the concen- anthropogenic, but rather a consequence of the nutrient-like
trations measured in this study, a 60 kg adult could only eat 160 g biogeochemical cycle of Cd which is linked to the high primary
a week of the mussels with the lowest concentration of Cd found in production in the GOC. With the exception of the high and min-
this work (Punta Estrella), but only 28 g a week of the mussels with ing-related concentrations of Co, Cu, Pb, and Zn found in the area
the highest concentrations (San Francisquito). If we consider that of Santa Rosalia, most of the stations showed sediments with low
the mean tissue weight for one mussel (based on the organisms trace metal concentrations and, excluding Cd, low enrichment
collected in the present study) was 21 g, a 60 kg person could only factors (EFMe < 1).
eat 3 or 1 organisms per week of the lowest and highest Cd concen- In general, the Cd geoaccumulation indexes (Igeo; Müller, 1979)
trations, respectively. Even though our results suggests that the suggest that pollution levels were from moderate to severe. Since
high Cd concentrations found in mussels in this study are not of mussels accumulate only the bioavailable fraction of metals, Cd
anthropogenic origin, but rather due to natural processes, the max- enrichments in sediments (total fraction) were not necessarily re-
imum concentration found in San Francisquito (117 lg g1 dw) flected in the organism tissue. In contrast, even when Mn, Fe, and
was nine times the highest concentration of 13 lg g1 dw reported Zn were found to be impoverished in sediments, their concentra-
for the west coast of the United States by Kimbrough et al. (2008). tions were the highest in mussel tissues. Our results suggest that
In general, GOC mussels have on average four times the amount of intake of sedimentary particulate material and its accumulation
80 A. Muñoz-Barbosa, M.A. Huerta-Diaz / Marine Pollution Bulletin 77 (2013) 71–81

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