Arch Environ Contam Toxicol DOI 10.1007/s00244-008-9210-x
Spatial Variability of Trace Metals and Inorganic Nutrients in Surface Waters of Todos Santos Bay, Me´xico in the Summer of 2005 During a Red Tide Algal Bloom M. L. Lares Æ S. G. Marinone Æ I. Rivera-Duarte Æ A. Beck Æ S. San˜udo-Wilhelmy
Received: 22 January 2008 / Accepted: 21 July 2008 Ó Springer Science+Business Media, LLC 2008
Abstract Dissolved and particulate metals (Ag, Cd, Co, Cu, Ni, and Zn) and nutrients (PO4, NO3, and H4SiO4) were measured in Todos Santos Bay (TSB) in August 2005. Two sources producing local gradients were identified: one from a dredge discharge area (DDA) and another south of the port and a creek. The average concentrations of dissolved Cd and Zn (1.3 and 15.6 nM, respectively) were higher by one order of magnitude than the surrounding Pacific waters, even during upwelling, and it is attributed to the presence of a widespread and long-lasting red tide coupled with some degree of local pollution. A clear spatial gradient (10 to 6 pM), from coast to offshore, of dissolved Ag was evident, indicating the influence of anthropogenic inputs. The particulate fraction of all metals, except Cu, showed a factor of *3 decrease in concentrations from the DDA to the interior of the bay. The metal distributions were related to the bay’s circulation by means of a numerical model that
shows a basically surface-wind-driven offshore current with subsurface compensation currents toward the coast. Additionally, the model shows strong vertical currents over the DDA. Principal component analysis revealed three possible processes that could be influencing the metal concentrations within TSB: anthropogenic inputs (Cd, Ag, and Co), biological proceses (NO3, Zn, and Cu), and upwelling and mixing (PO4, H4SiO4, Cd, and Ni). The most striking finding of this study was the extremely high Cd concentrations, which have been only reported in highly contaminated areas. As there was a strong red tide, it is hypothesized that the dinoflagellates are assimilating the Cd, which is rapidly remineralized and being concentrated on the stratified surface layers.
Introduction M. L. Lares (&) Departamento de Oceanografı´a Biolo´gica, CICESE, P.O. Box 434844, San Diego, CA 92143-4844, USA e-mail:
[email protected] S. G. Marinone Departamento de Oceanografı´a Fı´sica, CICESE, San Diego, CA 92143-4844, USA I. Rivera-Duarte Environmental Sciences and Applied Systems, Code 2375, SPAWAR Systems Center, San Diego, CA, USA A. Beck Marine Sciences Research Center, Stony Brook University, Stony Brook, NY 11794-5000, USA S. San˜udo-Wilhelmy Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371, USA
Todos Santos Bay (hereafter TSB) located in Baja California in the northwest part of Me´xico (see Fig. 1) is a small bay facing the California current system. The major oceanographic feature influencing the marine ecology off the Baja California coast is upwelling events that occur throughout the year (although they are more intense during spring and summer; Bakun and Nelson 1977; Barton and Argote 1980; Torres-Moye and Acosta-Ruiz 1986). These events have been detected by means of Cd measurements in mussels and seaweeds (bioindicator organisms) at San Quintı´n, 200 km south of TSB (Lares et al. 2002) and at Punta Banda, located just outside TSB (Segovia-Zavala et al. 2004) (Fig. 1). Although several hydrographical parameters suggest that upwelling events transport middepth waters from the California current system into TSB (Espinosa-Carreo´n et al. 2001), the impact of this transport
123
Arch Environ Contam Toxicol
USA
BTS 31.9 1
SQ
2
México
3
4
5
DDA 6
7
8
o
Latitude N
Port
31.8
Todos Santos Bay 10
9 12
13
10 km −116.8
11 14
10 km
31.7
R
Pacific Ocean
15
PB
*
−116.7
−116.6
Longitude o W
Fig. 1 Study area: Todos Santos Bay. The dots and figure over them indicate the location of the respective stations where water samples for trace metals and nutrients were collected. PB and SQ stand for Punta Banda and San Quintı´n, respectively. DDA indicates the area where the dredging material from the port and navigation channels is
discharged. The line labeled R stands for a small seasonal stream (Arroyo El Gallo) that discharges to the bay. The asterisk to the south of Punta Banda is Puerto Escondido, where some results are reported in the text
on the chemical and physical properties of surface waters of TSB is still unclear. Different processes such as remobilization from contaminated sediments, biological uptake, anthropogenic sources, and water mass transport affect the distribution of trace metals in coastal waters. The concentration and distribution of several trace metals have been used as indicators of those processes. For example, it is well known that Cd is a good upwelling indicator (Bruland et al. 1978; de Baar et al. 1994; van Geen and Husby 1996) and Ag is considered a good anthropogenic (sewage-derived) tracer (San˜udo-Wilhelmy and Flegal 1992). Copper and Ni are influenced by diagenetic remobilization and by upwelling processes (San˜udo-Wilhelmy and Flegal 1996). Although several studies have reported on trace metals concentrations in coastal waters off Baja California (e.g., San˜udoWilhelmy and Flegal 1991, 1992, 1996; Segovia-Zavala et al. 1998), no study has addressed the spatial variability in the concentrations of trace metals in TSB waters. During the last few years, TSB and all along the Baja California and California coast, harmful algal blooms have been occurring more frequently; in particular, the summer of 2005 experienced a long-lasting red tide (April to September; Pen˜a-Manjarrez et al. 2008). The physical environment in the northern California currents exhibited highly anomalous conditions of upwelling resulting in elevated surface temperatures relative to all previous recorded summers (Brodeur et al. 2006). Also, Pierce et al. (2006) reported a delayed cold temperature of about 6 weeks in the US–Canada Pacific. Here are reported some trace metal concentrations in TSB during August when the red tide algal bloom was still present. The objective of this work was to study the spatial variability of dissolved and particulate metals (Ag, Cd, Co,
Cu, Ni, and Zn) and nutrients (PO4, NO3, and H4SiO4) in the surface waters of TSB and to identify some of the firstorder processes (e.g., upwelling, surface circulation, etc.) that could explain the spatial gradients by means of a circulation numerical model.
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Material and Methods Trace Metals and Nutrients Samples were collected at 15 locations within TSB (Fig. 1) on August 10, 2005 at 1 m below the surface and in the upstream side of the R/V Genus, using a 2-m-long PVC pole (made for this purpose) that enables one to open and close the bottles underwater. The sampling team followed a ‘‘clean-hands/dirty-hands’’ protocol. Bottles were previously trace-metal cleaned and double zip-lock bagged. Immediately after recovery, the sample bottle was place back by a ‘‘clean-hands’’ person. All of the samples were collected within 4 h to avoid any bias caused by tide phase change. All of the analyses were carried out in a HEPA-filtered clean room. Seawater was prefiltered through a precleaned (acid washed) 1-lm Nucleopore filter (47-mm diameter), as the amount of particles due to the red tide plugged the 0.45-lm (47-mm-diameter Nucleopore) filters very quickly. Dissolved metals in this study are defined as those that pass through a 0.45-lm filter. Filtered seawater was acidified (pH \ 2.0) with Ultrex-grade nitric acid and preconcentrated with ammonium 1-pyrrolidinedithiocarbamate/diethylammonium diethyldithiocarbamate (APDC/ DDDC) in an organic extraction for Ag, Cd, Co, Cu, Ni, and Zn. Cadmium was preconcentrated again using the
Arch Environ Contam Toxicol
Chelex-100Ò (Bio-Rad Laboratories, Richmond, CA) ionexchange technique (Bruland et al. 1979). Filters (1 and 0.45 lm) were digested using a combination of HNO3, HCl, and HF in Teflon digestion bombs at 100°C according to the technique described by Eggimann and Betzer (1976). All dissolved and particulate metals were quantified by inductively coupled plasma–mass spectrometry (ICP-MS) (Element 2) using established protocols (Cullen et al. 2001). Cadmium concentrations (after Chelex-100 preconcentration) were also determined by graphite furnace– atomic absorption spectrometry (GF-AAS; AAnalyst 600, Perkin-Elmer Inst.), using stabilized platform techniques and the method of standard additions to correct for matrix interferences. The accuracy of the analytical protocols ranged from 97% for Ni to 106% for Cd, based on the analysis of the standard reference material Cass-3 (Canadian Research Council Canada). The variations of replicate analyses were 9%, 9%, 25%, 6%, 11%, and 6% for Cd, Ag, Zn, Cu, Co, and Ni, respectively. Analytical detection limits were 0.25, 9, 5, 170, 300, and 500 pM for Ag, Cd, Co, Cu, Ni, and Zn, respectively. In order to gain understanding of the spatial gradients in metal concentrations, levels of dissolved inorganic nutrients (NO3, PO4, and H4SiO4) were also measured. Concentrations were determined with a Skalar San Plus System II autoanalyzer by measuring the absorbance induced by chromatic complexes (Eaton et al. 2005).
establish the TSB’s circulation during the sampling. The best bathymetry of the region allowed a model domain mesh size of 556 9 470 m in the horizontal; in the vertical, 16 layers were chosen in order to have enough resolution of the interior and exterior of the bay. The model equations are solved semi-implicitly with fully prognostic temperature and salinity fields, thus allowing time-dependent baroclinic motions. The model has been successfully used by us and other authors in many different domains and conditions and the reader is referred to the literature for more information (e.g., Marinone 2003, and references therein; Marinone and Pond 1996; Stronach et al. 1993). The simulation reported here is forced with tides and wind only. A NW wind of *5 m/s imposed, which is parallel to the coast, as it was locally observed (see ftp://ftp.cicese.mx/pub/divOC/ ocefisica/vientos/sauzal/MET/2005) and in agreement with the SeaWinds Scatterometer aboard the QuikSCAT satellite (see http://manati.orbit.nesdis.noaa.gov/quikscat/). For the tidal forcing in the open boundaries, the harmonic constants were obtained from the regional model WC3 of the Oregon University for the Pacific Ocean (http://www.coas.oregon state.edu/research/po/research/tide/region.html). The initial hydrographic structure consists of a simple stratified water column based on the climatology, but as mentioned earlier, the temperature and salinity fields are allowed to evolve.
Results and Discussion Numerical Model In order to determine whether metal distributions in TSB were influenced by advective processes, the HAMSOM three-dimensional baroclinic numerical model was used to
A summary of the concentration of the different variables measured (metals only the dissolved fraction) is given in Table 1. Averages and maximum and minimum values are listed together with some values obtained from the
Table 1 Mean, maximum, and minimum values of nutrients and dissolved metal concentrations measured in this study Mean
Maximum
Minimum
North Pacific 0–0.1 (a)
Pacific Coast
TSB
10.8–16.2 (b)
0.2–2 (c)
NO3
2.61
17.00
0.77
PO4
1.40
5.11
0.51
0.02–1.60 (d)
0.5–2.5 (e)
H4SiO4
5.08
7.03
3.07
2.7–32.2 (d)
5–50 (e)
Cd
1.30
2.15
0.46
0.04–0.16 (a)
Ag
6.93
10.79
3.64
1–2.4 (i)
Zn
15.61
71.05
5.62
0.13–0.48 (l)
Cu
2.41
3.58
1.88
Co
0.30
0.56
0.16
Ni
3.80
4.36
3.26
0. 1–1.0 (g) 6–18 (j)
0.5–1.0 (c) 4.2 (f) 0.10–0.16 (h) 5–26 (k)
0.2–1.9 (m)
NA, 20 SFB (n)
0.43–1.46 (o)
0.9–1.9 (h)
2.14–3.60 (h)
0.07–0.13 (p)
0.04–0.11 (q)
0.11–0.38 (h)
2.2–10 (a)
4.5–5.6 (n)
3.40–3.68 (h)
Note: Some reference values from the literature (not exhaustive) are shown for comparison. Units are in micromolars for nutrients and in nanomolars for all metals except for Ag (pM). Note that for Zn there is no available (NA) data for TSB; instead, values for San Francisco Bay (SFB) are reported. Bold values indicate that are higher than expected Sources: (a) Bruland 1980; (b) Fitzwater et al. 2003; (c) Espinosa-Carreo´n et al. 2001; (d) Boyle et al. 1976; (e) van Geen and Luoma 1993; (f) ´ lvarez-Borrego 1984; (g) Takesue et al. 2004; (h) San˜udo-Wilhelmy and Flegal 1996; (i) Martin et al. 1983; (j) Flegal et al. Gaxiola-Castro and A 1991; (k) San˜udo-Wilhelmy and Flegal 1992; (l) Bruland et al. 1978; (m) San˜udo-Wilhelmy and Flegal 1991; (n) (o) Coale and Bruland 1990; (p) Martin and Gordon 1988; (q) Johnson et al. 1988
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Arch Environ Contam Toxicol Fig. 2 Spatial distribution of PO4, NO3, and H4SiO4 in TSB during August 2005. Note that a very high value of NO3 in the southwestern corner is indicated
(a) PO4 [µM]
(b) NO3 [µM]
1
1.6 1.2 1.6
2 3
4
2
1
1.2
2
1
1.6
2
1.6
17!
(c) H4SiO4 [µM]
5
6
7 5
literature for oceanic and coastal waters of the Pacific; also, previous values reported for TSB are included. Most of the concentrations of the different parameters obtained in this study were within the range reported for coastal waters and TSB. However, the upper limit of the concentrations of PO4, Cd, and Zn (bold in Table 1) were higher than those previously reported for coastal and open ocean waters of the northeast Pacific and for TSB (except for Zn because there are no available data for the bay). The spatial distribution of inorganic nutrients (PO4, NO3, H4SiO4) is shown in Fig. 2. Nitrate was found at low concentrations (0.77–2.73 lM), similar to those previously reported by Espinosa-Carreo´n et al. (2001) for TSB but very low if they are compared to upwelled waters ([10 lM). These low concentrations were expected because nitrate is the limiting nutrient for phytoplankton and a red tide was occurring in TSB during the sampling (Pen˜a-Manjarrez et al. 2008). The highest nitrate concentrations were found by the Port facilities near the discharge of Arroyo El Gallo (a seasonal stream labeled R in Fig. 1). Just one very large value at station 12 was found (the two replicate samples have 18.5 and 15.6 lM of NO3), which contrasts with the rest of the bay. Dissolved silicate and phosphate were higher in the exterior stations (just north of the island: stations 3 and 6), reflecting the upwelling and mixing that occurs in this zone (see below). In this area, the dredged sediments being removed from the port are discharged (Romero-VargasMa´rquez 1995) and, thus, these increased values of H4SiO4 and PO4 could be the result of resuspension and dissolution
123
4
of this material. This region will be referred as the dredge discharge area (DDA) that is around stations 3 and 6. Also in this area, there is a relative shallow bank of *35 m depth surrounded by a *50 m water column, thus inducing internal tides and vertical mixing. In a study on metals distribution in sediments within TSB, Romero-Vargas-Ma´rquez (1995) reported the highest concentrations of several metals, including Cd, Cu, Zn, and Ni in the DDA and inside the port. Furthermore, in a study in which sediment samples were collected along the coast of Baja California from the Me´xico-USA border to TSB, Sandoval-Salazar (1999) reported that the most metalenriched sediments (e.g., Cd, Ag, Cu, Pb, and Zn) were localized around TSB islands. The Cd spatial distribution of the dissolved and particulate fractions is shown in Fig. 3a, b. Cadmium was dominated by the dissolved fraction with values up to 2.15 nM. This fraction had high levels in both the interior and exterior areas of the bay. Dissolved Cd concentrations were one order of magnitude higher compared to concentrations previously reported for one point inside the bay close to station 11 (0.16 nM; San˜udo-Wilhelmy and Flegal 1996) and 40 times compared to nutrient-depleted surface waters of the California Current (0.05 nM; Bruland 1980). Previous samples taken during 2001–2002 (Lares, unpublished data) in the surf zone in eight locations around TSB (including the island) showed maximum Cd concentrations of 0.51 and 0.47 nM close to Arroyo el Gallo and inside the port, respectively.
Arch Environ Contam Toxicol Fig. 3 Spatial distribution of Cd and Ag in Todos Santos Bay during August 2005. The dissolved and particulate fractions are shown in the left and right panels, respectively
(a) Cd Diss [nM]
(b) Cd Part [nM]
1
0.3
1.5 2
5
1
1.
2
1
0.5
5 1.
0.3
0.3 0.1
0.5
(c) Ag Diss [pM]
(d) Ag Part [pM]
8
6
9
5
7
The unexpected high values of Cd are consistent with the high PO4 concentrations found. The concentrations of this inorganic nutrient were also up to five times higher (5.11 lM) than those reported for TSB during upwelling season (1.0 lM; Espinosa-Carreo´n et al. 2001). Increases of PO4 in the late period of a bloom have been reported (Baetje and Michaelis 1986). The slope of the Cd:PO4 relationship obtained (Cd = 0.79 ? 0.36 9 10-3 PO4; r = 0.695) was similar to that found by de Baar et al. (1994) for deep ([1000 m) North Pacific waters (0.33 9 10-3); the correlation was significant (p = 0.006). Taking out the extreme PO4 value (5.11 lM) found at station 6 (close to DDA), the slope of the Cd:PO4 increased (Cd = 0.36 ? 0.78 9 10-3 PO4; r = 0.814) and the correlation was highly significant (p = 0.001). Usually, the Cd:PO4 ratio is lower in surface waters than in deep waters, which is consistent with preferential biogeochemical removal of Cd versus phosphate from surface waters (de Baar et al. 1994). The high Cd:PO4 ratio found here implies that Cd has been preferentially removed by the phytoplankton and remineralized in the stratified waters. A seasonal thermocline is formed during April–August at TSB each year, ranging from 4 to 8 m in depth (Pen˜aManjarrez et al. 2008). As previously mentioned, the red tide lasted from April to September; therefore, the sampling occurred in the late period of the bloom. The concentrations of particulate Cd seems to correlate with several sources of contaminants, as the highest levels
10
10
9
5
7 6
8
5
15
7
6 5
10
were found near the DDA (stations 3 and 6), by the local marina (station 5, Fig. 1) and south of the Port facilities (stations 11 and 14). Low metal values (dissolved and particulate) are found to the south of TSB and close to Punta Banda (PB) (stations 12, 13, and 15). The spatial distribution of the dissolved and particulate Ag is shown in Fig. 3c, d. Dissolved Ag decreased toward the exterior of TSB by *50%, suggesting the influence of anthropogenic sources near the shore. The particulate fraction increases by a factor of *3 from the south/center region of TSB toward the western area of the bay and over the DDA where resuspension and transport to the surface by a mechanism such as tidal currents and upwelling is occurring. In general, the lower values were found to the south part of TSB close to PB, as observed for Cd (Fig. 3a, b). The concentrations of dissolved Ag (4–11 pM) measured in this study were consistent with the concentration range (5–26 pM) and gradient (low outside, high inside the bay) reported by San˜udo-Wilhelmy and Flegal (1992) for few stations within TSB. The distributions of Zn and Cu are shown in Fig. 4. The highest concentrations of both dissolved metals (and NO3) were detected toward the southern entrance of TSB and particularly at station 12, where 70 nM of Zn were found. For Cu, there is also an increase in concentration (for both particulate and dissolved fractions) toward station 5, which is located just in front of the tourist marina. High levels of Cu (and Zn) near marinas is consistent with the high
123
Arch Environ Contam Toxicol Fig. 4 Spatial distribution of Zn and Cu in Todos Santos Bay during August 2005. The dissolved and particulate fractions are shown in the left and right panels, respectively
(a) Zn Diss [nM]
(b) Zn Part [nM] 10
10
10
10 5
20 5400 30
10
20
15
(c) Cu Diss [nM]
(d) Cu Part [nM] 0.8
2
1.6 1.2 0.8
4 2. 2.8 3.2
0.4
2.4
2
2
2.4
Fig. 5 Spatial distribution of Co and Ni in Todos Santos Bay during August 2005. The dissolved and particulate fractions are shown in the left and right panels, respectively
(a) Co Diss [nM]
(b) Co Part [nM] 0.2 0.25 0.3 0.35 0.4
0.3 4 0.
0.35 0.3
0.3
0.3
0.2
5 0..34 0
0. 4 0.55
0.25
5
0.2
(d) Ni Part [nM]
3.
75
1
4.25
1.2
4
4
3.5
3.75
1.2 1.4
1
0.8
6 0.
5
content of Cu in maritime paints and the use of Zn in the manufacturing of anodes for boat motors (Breuer et al. 1999). The general distribution of dissolved and particulate Zn in the rest of the bay has a tendency to have large values toward the DDA in the exterior of TSB similar to the
123
0.2 0.2 5
0.1
(c) Ni Diss [nM]
3.7
0.15
patterns observed for dissolved and particulate Cd and particulate Ag. The geographical distributions of Co and Ni are shown in Fig. 5. Dissolved Co has a distribution similar to that observed for dissolved Ag. Particulate Co and both Ni
Arch Environ Contam Toxicol
fractions have a similar distribution pattern with high values toward the exterior and near to shore southeastern areas of the TSB, similar to Cd distributions. The metal and nutrient distributions observed in TSB during this study can be summarized as follows: (1) metals and nutrients whose concentrations decrease from the DDA to the interior of the bay (all particulate metals except Zn and dissolved Cd, Ni, H4SiO4, and PO4), (2) metals and nutrients whose concentrations decreased from the port/ Arroyo el Gallo and eastern coastal areas toward the interior and south of TSB (all particulate metals except Zn and dissolved Cd, Ag, Co, and PO4). In the first case, the large surface concentration suggests that the material dumped to the bottom in the DDA has been resuspended and transported to the surface by a mechanism such as tidal currents interacting with the shallow bank close to the DDA and upwelling due to the NW winds that were persistent during August (as mentioned earlier). A similar mechanism (resuspension–upwelling) has been invoked to explain high levels of dissolved Fe off Monterey Bay (Johnson et al. 1999). In the second, a transport to the south might be implied. Little is known about the bay’s circulation: Argote et al. (1991) predicted anticyclonic (cyclonic) circulation in response to NW (S) winds, based on a vertically integrated numerical model with significant speed only close to the coast. This model result has been validated by empirical ´ lvarez-Sa´nchez et al. 1988). data generated with drifters (A In contrast to the Argote et al. (1991) model, our model simulation provides a more detailed circulation pattern because it is three dimensional. The model was validated
2 1.5 1 0.5 0 −0.5 −1 −1.5 −2
0
100
200
300
400
500
600
700
Fig. 6 Tidal elevation (meters) in the port of Ensenada. The broken line corresponds to the tidal prediction from the observations and the solid line to the model calculation. The horizontal axis is in hours of 1-month run
by comparing the predicted tidal elevation at the Port superimposed to that computed by the model (Fig. 6). These preliminary results show that the tide is well reproduced, validating the model outcomes. The instantaneous currents are a combination of that induced by the wind and the oscillatory tidal currents. Figure 7 shows the time-averaged or residual currents for the indicated model layers. The contours in Fig. 7a represents the bathymetry of TSB, and in Fig. 7b–d, the contours represent the vertical velocity in the top of the corresponding layer. Tidal
Fig. 7 Residual (tide and wind induced) currents in Todos Santos Bay for the different model layers. The contours represents the bathymetry in meters (a), and in the rest, the vertical velocity on top of the indicated layer in meters per day
123
Arch Environ Contam Toxicol
currents are important only in the interior layers and close to the coast (especially to the south of the bay), being larger than those induced by the wind and able to reverse the circulation (not shown). The general circulation pattern obtained with our model (Fig. 7) is more complicated than that obtained with the simple depth-averaged model of Argote et al. (1991). As expected, the surface layer is clearly wind driven, with an offshore Ekman transport and with currents following also the coastline. South of the Port, the currents are also to the south and could transport contaminants from the port/creek as observed in the metal distributions. The DDA region is located precisely where the stronger upward vertical velocity is produced by the model, which validates the hypothesis that contaminants in the dredge material is being transported from the bottom to surface waters. In the southern region of TSB, the residual currents are weaker, but the instantaneous tidal currents are strongest (Mateos et al. 2008). There, the currents over the canyon (more than 300 m in depth) between the island and Punta Banda produces both internal tides and large tidal excursions. The internal tide propagates and might break toward the shallower bathymetry and the large tidal excursion must impinge over the slope also toward the interior of the southern part of the bay. It was expected that the deep waters from the canyon have more oceanic metal concentrations than inside the bay. This advection/dilution mechanism might explain the low values of all metals (except dissolved Ni) observed in that region. It has been shown that the spatial distribution of trace metals (with the exception of dissolved Ni) within TSB seems to be influenced by the internal water circulation. In order to find a relation among different variables (metals, nutrients), a correlation analyses among particulate metals, dissolved metals, and nutrients was performed. A principal component analysis was also performed between dissolved metals and nutrients. Within the particulate fraction, all of the metals were significantly correlated with particulate Ag (Table 2); also, most of the other metals were significantly related among them. Therefore, the distributions of all particulate metals (but Cu) can be explained by the zone of
Table 2 Correlations among the particulate fraction of metals Cd
Ag
Zn
Co
Cu
Ni
Cd
0.849
0.618
0.666
0.325
0.467
Ag Zn Co Cu
0.572
0.791
0.575
0.698
0.382
0.361
0.333
0.828
0.661 0.793
Note: Bold figures correspond to correlations significant to the 95% confidence limit (CL) (n = 15)
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Table 3 Principal component analysis Var
C1
C2
C3
NO3
-0.13
-0.95
-0.02
PO4
0.31
0.21
0.82
-0.30
0.11
0.78
H4SiO4 Cd
0.81
0.02
0.53
Ag
0.83
-0.18
-0.24
Zn
-0.11
-0.95
0.07
Cu
0.38
-0.68
-0.11
Co
0.94
0.18
0.06
Ni
0.04
-0.27
0.88
Explained variance (%)
32
27
24
Interpretation
Anthropogenic
Biological uptake
Physical procesess (mixing, upwelling)
Note: Metals are from the dissolved fraction. Bold figures correspond to loads higher than 0.5
mixing/upwelling found around the DDA. The Cu distribution can be explained by the input of particulate Cu from the port/marina region. The correlation analyses for the dissolved metals and nutrients were not as clear and therefore principal component analyses (PCAs) were performed with all of the constituents measured in that pool. PCAs unravel more clearly the relationship of dissolved metals and nutrients (Table 3). The three most important components, which account for 83% of the variance, groups Cd, Ag, and Co in the first component (which explains only 32% of the variance); which can be interpreted as the influence of the anthropogenic inputs on the distribution of these metals, given that dissolved Ag is a recognized tracer (San˜udoWilhelmy and Flegal 1992) that can be widely dispersed around anthropogenic input sources (Luoma et al. 1995). The second component (27% explained variance) relates NO3, Zn, and Cu, which translates into biological uptake, as these three dissolved constituents are essential to phytoplankton (Morel and Price 2003). Probably Zn and Cu are in higher amounts than are essential for phytoplankton; however, their relation with a limiting nutrient such as NO3 and the widely distributed and long-lasting red tide present suggests that there is a biological process involved. The third one (24% explained variance) relates PO4, H4SiO4, Cd, and Ni, which could be interpreted as a factor that describes the influence of physical processes such as upwelling and mixing. Cadmium, PO4, and H4SiO4 are sensitive indicators of upwelling (van Geen and Husby 1996). The strong linear relationship of Cd with PO4 due to its involvement in phytoplankton production and remineralization, as previously discussed, is reflected here. The relation between Cd and H4SiO4, on the other hand, is not
Arch Environ Contam Toxicol Table 4 Dissolved Cd and phytoplankton abundances for the indicated dates during 2006
Note: TSB and PE stands for Todos Santos Bay and Puerto Escondido, respectively
Location
Date
Cd conc. (nM)
TSB
May 9
2.05
8,000
237,000
PE
June 1
0.49
19,000
66,500
PE
June 30
0.01
84,000
10,000
PE
July 31
0.90
181,500
76,000
PE
September 1
0.25
154,700
7,400
linear (second-order polynomial; van Geen and Husby 1996), which indicates an uncoupled regeneration (slower for Si) in the water column. This can probably explain the lower concentrations of H4SiO4 compared to PO4. Finally, the most striking result of this study is the extremely high concentrations of Cd found. The interpretation is that they are related to the red tide because, as previously mentioned, we have measured concentrations less than 0.6 nM within the bay, but no red tide was present. Additionally, recent measurements (2006) of dissolved Cd and phytoplankton (diatoms and dinoflagellates) abundance (Valdez-Ma´rquez, 2008, Programa de Monitoreo de Maricultura del Norte, Ensenada, Me´xico, Unpublished report) from samples taken in TSB and in Puerto Escondido (see Fig. 1) showed high dissolved Cd concentrations (similar to those reported here) coupled with high dinoflagellates abundance (Table 4). Furthermore, the correlation between these two variables was highly significant (r = 0.982, p = 0.003). These Cd concentrations however, were not related to diatom abundance (r = - 0.409, p = 0.495; Table 4). Sakaguchi et al. (1979) found that the ability of a range of green algae to accumulate Cd was species-specific. Additionally, Abe and Matsanagu (1988) in culture experiments showed that Cd-PO4 removal from seawater was dependent on the plankton species as well as the Cd:PO4 relation in the euphotic zone. In TSB red tide event (April– September, 2005) Pen˜a-Manjarrez et al. (2008) reported that it was dominated by dinoflagellates. It is hypothesized that during this time the dinoflagellates assimilated Cd, which was rapidly remineralized and accumulated to a high degree in the stratified surface layers of TSB due to the long-lasting red tide event that occur in 2005. Acknowledgments This research was financed by CONACYT, through grant 44055 of SGM and by CICESE’s regular budget. We also thank Marcos David Martı´nez Gaxiola for the nutrient analyses.
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