Research Articles

Polychlorinated Biphenyls in Mussels

Research Articles

Polychlorinated Biphenyls (PCBs) in Mussels along the Chilean Coast Gonzalo Mendoza1*, Luis Gutierrez2, Karla Pozo-Gallardo3, Daniel Fuentes-Rios1, Monica Montory1, Roberto Urrutia1 and Ricardo Barra1 1Aquatic

Systems Research Unit, EULA-Chile Environmental Sciences Center University of Concepción, Chile of Statistics, Faculty of Mathematics and Physical Sciences, University of Concepción, Chile 3Meteorological Service, Environment Canada, Canada 2Department

* Corresponding author ([email protected])

In memory of Davide Calamari Introduction

DOI: http://dx.doi.org/10.1065/espr2006.01.011 Abstract

Goal, Scope and Background. Chile signed the Stockholm Convention, which establishes measures to reduce or eliminate Persistent Organic Pollutants (POPs) release into the environment, including the prohibition of their use and reduction of secondary products release, as well as management related with waste treatment. Among POPs, PCBs are a family of 209 compounds that differ in chlorine level and position. These substances present a wide variability in their physicochemical properties such as vapor pressure, water solubility and partition coefficients that determine their behavior and mobility within the different environmental compartments. In Chile, as in other countries, the use of these compounds were and continue to occur in diverse industrial applications such as dielectric fluid in transformers and condensers, with a use in Chile of approximately 550,000 L. A sampling of bivalves was performed during the years 2000-2002 in order to obtain information on the spatial distribution of the PCB levels for the length of the long Chilean coast (180–540 South latitude, 4,200 km), contributing in this way to a better understanding of the PCB trend and eventual fractionation along latitudinal gradients in Chile, using as the bivalve Perumytilus purpuratus ('Chorito Maico') bioindicator. Methods. The marine bivalves Perumytilus purpuratus were collected in 16 localities in northern and southern Chile. All samples were lyophilized, and PCBs (51 congeners) were extracted in a Soxhlet system (24 h) with n-hexane. Samples were cleaned in florisil and analyzed by GC-ECD. Blanks, certified reference materials and standards were processed along with the samples. Results and Discussion. The results obtained for P. purpuratus indicate a congeneric distribution profile associated to a latitudinal gradient, and the statistical analysis of the congeneric composition of the PCBs indicated five groups in relation to the molecular weight (number of chlorines), where the lighter congeners were observed in areas corresponding to high latitudes with total PCB values of 298 ng/g dry weight. Conclusion. P. purpuratus turns out to be a good bioindicator of PCB levels in the coastal areas of Chile due to its wide distribution. The highest concentrations and the more volatile congeners were found in southern Chile, which could be the result of processes of long-range transport or illegal discharge occurring in such remote areas. These results confirm previous data from the International Mussel Watch project ten years ago. Recommendation and Outlook. Future studies are needed to confirm our findings utilizing another environmental matrix such as soil/sediments and air samples. Keywords: Chile; long-range transport; mussels; persistent organic pollutants (POPs); Perumytilus purpuratus; polychlorinated biphenysls (PCBs)

Persistent Organic Pollutants (POPs) are a global environmental issue in part due to the massive use, continued emission and toxicity, bioaccumulation potential, and persistence and mobility throughout the environment. The mobility characteristic has resulted in their detection even in remote areas of the Polar Artic (Iwata et al. 1994, Stern et al. 1997) and Antarctic regions (Bidleman et al. 1988, Focardi et al. 1991, Ockenden et al. 2001). In general, even though the environmental POP levels are lower in the Southern than in the Northern Hemisphere, the behavior and fate of these chlorinated compounds are not understood, in part due to the inadequate source characterization and the lack of monitoring efforts (Barra et al. 2005). Within POPs, this study is interested in PCBs. The synthesis of these compounds was described for the first time in 1881 and its commercial production begins at the end of 1920 (UNEP 2002), specifically between 1929 and 1993. Total global production has been estimated to reach 1.3 million tons (Breivick et al. 2002). In Chile, as in other developing countries, PCBs have been used for over 30 years in many different industrial applications (Barra et al. 2004a), principally as dielectric fluid, which was prohibited in 1982 only in new transformers and condensers. However, their use in old devices and later storage may present a high environmental risk. In July 2004, Chile ratified the Stockholm Convention, which established different measurements to reduce and to eliminate POPs, including the prohibition of use and reduction of liberation of by-products. This agreement has served as a diagnostic and assessment mechanism for these compounds at the national level. The first national inventory of PCBs was finalized, finding a minimum total amount of PCBs of 569,547 L, of which 327,005 L are in use and 242,542 L are stored (CONAMA 2005, in press). Among the characteristics of the PCBs, one of the most important is a wide variability in their physical-chemical properties (vapor pressure, water solubility and partition coefficients) due to their great number of congeners (209), varying from very slight compounds, such as monochlorobiphenyl, to a not very volatile compound such as decachlorobiphenyl, which determines their behavior and mobility in the different environmental compartments.

ESPR – Environ Sci & Pollut Res 13 (1) 67 – 74 (2006) © 2006 ecomed publishers (Verlagsgruppe Hüthig Jehle Rehm GmbH), D-86899 Landsberg and Tokyo • Mumbai • Seoul • Melbourne • Paris

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Polychlorinated Biphenyls in Mussels

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Biomonitoring has been used as a strategy to evaluate spatial and temporal trends and POP environmental trends. Calamari et al. (1991) were the first group to identify an inverted concentration gradient of hexachlorobenzene in leaf samples from different species coming from many sites around the world. All these data, together with evidences of PCB concentration and compositions detected in fish liver in Canadian rivers and lakes (Muir et al. 1990), were key in providing the support data for the hypothesis of global POP fractionation (Wania and MacKay 1993). Although the existing information that supports this hypothesis comes principally from the Northern Hemisphere (Ockenden et al. 1998, 2001), the lack of basic information from the Southern Hemisphere has been recognized. Indeed, the absence of quantitative data and the lack of a historic database of PCB use in the Southern Hemisphere (Barra et al. 2004a) inhibit the reconstruction of environmental trends of PCB levels during the last 50 years. Bivalves have been widely used to assess the temporal and spatial PCB contamination trends (Prest et al. 1994, Kurt and Ozkoc 2004, Potrikus et al. 2003) because these invertebrates present characteristics and advantages that make them particularly useful to analyze the impacts of these pollutants on marine ecosystems: They (a) present a wide geographic distribution, (b) a low degree of detoxification activity, (c) are sessile organisms during most of their life cycle, (d) and finally, live in the rocky intertidal shore, where the contamination problems generally take place (Viarengo and Canesi 1991, Regoli and Principato 1995). Consequently, they give a temporary integrating measurement of PCB concentrations due to the bioaccumulation processes, providing bioavailability data for these pollutants (Cossa 1989, Salazar and Salazar 1998). In the South Hemisphere, specifically in Chile, the first report on the PCBs levels in marine organisms was the 'Mussel Watch Program', which at the beginning of the 90s ana-

lyzed samples of different bivalves from the American coast, including Chile (Sericano et al. 1995). Even though PCBs have been widely used at a global level, pollution monitoring in developing countries such as Chile is still lacking (Barra et al. 2004a). The goal of the present investigation was to provide information on the spatial distribution of the PCB levels for the length of the long Chilean coast (18°–54° South latitude, 4,200 km), contributing to a better understanding of PCB trends and eventual fractionation along latitudinal gradients in Chile. This aim was achieved by using the bivalve Perumytilus purpuratus ('Chorito Maico'), which is widely distributed in the Pacific Ocean from Ecuador to the Magellan Straits (Lozada and Reyes 1981) as a bioindicator. 1 1.1

Materials and Methods Sample collection

During the years 2000 and 2002 (summer), 30 to 40 individuals of P. purpuratus (maximum size extending from 30– 40 mm and weight between 4 and 6 g) were obtained in 16 localities in northern and southern Chile. These localities were selected either for the existence of nearby potential PCB sources (industries and cities) or for being remote areas, located far from direct pollution sources. All the samples were collected in the rocky, inter-tidal shore of each sampling site. Table 1 presents the geographic position of the sampling sites together with the characteristics and the average temperature following the coastline (MOP 1997). In each site, the bivalves were covered in aluminum paper, transported and stored at –20ºC in the laboratory for further analysis. For PCB analysis of the bivalves, the soft parts of the organism were used, thus avoiding that the constitution water of the organism was lost. All the samples were weighed before freezing, and then lyophilized during 48 h.

Table 1: Sampling Site Locations with Latitude/Longitude and total PCBs (ng/g d.w.)

Zone

Chile North

Sampling site

Chile South

Chile South End

68

Latitude W

Location

Total PCBs

Annual Average T° (°C) 17

Bewater

23° 36' 33''

70° 23' 35''

Urban area

15.37

Caleta Huanillo

23° 39' 00''

70° 24' 00''

Port of mining shipment

18.59

Caleta Coloso

23° 45' 00''

70° 28' 00''

Port of mining shipment

38.05

Playa Milico

23° 45' 21''

70° 28' 15''

Port of mining shipment

29.21

31° 39' 00''

70° 24' 00''

Remote area

19.69

32° 31' 00''

71° 27' 00''

Urban area

29.60

Zapallar

34° 03' 00''

71° 32' 00''

Urban area

62.38

Constitución

35° 18' 52''

72° 24' 56''

Urban area

10.20

Cocholgue

36° 30' 57''

72° 80' 00''

Urban area

13.59

Chile Playa Hipie Norte North Center Papudo Chile South Center

Latitude S

Lota

36° 56' 27''

73° 09' 09''

Urban area

13.41

C. Gonzalo

42° 51' 00''

71° 43' 00''

Remote area

12.01

Chaiten

42° 55' 00''

72° 43' 00''

Urban area

26.02

Huinay

42° 59' 00''

71° 56' 00''

Remote area

8.05

Punta Arenas I

53° 09' 00''

70° 55' 00''

Remote area

130.65

Punta Arenas II

53° 09' 50''

70° 54' 45''

Remote area

160.88

Punta Arenas III

53° 10' 10''

70° 55' 10''

Remote area

297.85

14

13

9

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1.2

PCB Analysis

Samples (2 g) were Soxhlet extracted with 100 ml of n-hexane for 24 hours, according to the methodology used by Focardi et al. (1996). The extracts were reduced for evaporation between 35 and 40ºC until 10 ml and then cleanedup with concentrated sulfuric acid for 24 hours at room temperature followed by florisil column chromatography (1 cm of internal diameter and 30-cm long stuffed with 5 g florisil), eluted with 100 ml n-hexane. For the identification, individual PCB congeners (51) were used, pertaining to 4 mixtures of the calibration standard, CLB-1 (CLB1-A, CLB1-B, CLB1-C and CLB1-D) purchased from the National Research Council Canada (NRCC). PCBs were analyzed by GC-ECD. Chromatographic conditions were the following: GC PERKIN ELMER Auto-system; Capillary column SPB5, Supelco 30 m x 0.25 µm x 0.25 mm; Injection port temperature 240ºC; Injection system split/splitless, Electron Capture Detector 63Ni (ECD) temperature 320ºC, Oven initial temperature 100ºC with Isotherms 10 min, Ramp rate, 5ºC /min to 280ºC, 56 min total time of the analysis. The Gas Carrier was He, and the Make up Gas Argon-methane (95:5). The PCBs were quantified using pentachloronitrobenzene (PCNB) as an internal standard, detection limits (2 g of sample) ranged between 3.09 and 6.66 ng/g dry weight depending on the congener. Data quality was evaluated using the same procedure for blanks, samples, standards and the reference material (NIST 2977, 25 PCB congeners), where the average recovery was above 65%, ranging from 52 to 105%. 2 2.1

Results and Discussion PCB concentrations and congener composition in gradient North-South

Fig. 1, Table 1 and Table 2 show the average of ∑PCBs concentrations ng/g dry weight (d.w.), the distribution of PCB congeners, expressed in % of Cl-groups and concentrations of PCB congeners obtained in 16 sites along the Chilean coast, classified in five sampling sectors according to their latitude (North, North center, South center, South and extreme South). Results obtained from the analysis of P.purpuratus indicate a distribution profile of lighter congeners associated with the North to South latitudinal gradient, with a temperature variation of 11ºC (17ºC, 23º latitude S; 6ºC, 53º latitude S) and concentrations fluctuating from 10 ng/g d.w to 298 ng/ g d.w. in the extreme South of Chile, where dichlorobiphenyl contributes an important percentage of the total mixture of PCBs in this area (PCB 15 and PCB 18). These results are in agreement with those found by Sericano et al. (1995) in the study of the International Mussel Watch Program, which reported a similar North-South gradient in seven locations in Chile, with higher PCB and Polycyclic Aromatic Hydrocarbon (PAHs) concentrations being found near the harbor of Punta Arenas.

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Polychlorinated Biphenyls in Mussels

2.2

Statistical analysis

The Principal Component Analysis (PCA) was used to examine the PCB congener variation and distribution (from 2Cl to 9-Cl congeners) in different sampling sites Statistical analyses were performed with STATISTICA 6.0 (this analysis was made for congener concentrations obtaining similar results). Analysis indicated five similar groups in all the sampling sites with exception of Lota and Chaiten. Fig. 2 presents the scores and Fig. 3 shows the loadings of every sampling site. The sites Huinay, Papudo and Caleta Gonzalo (Central-South Chile) show a clear predominance of 4-Cl congeners with 59%, 66% and 55%, respectively. However, 5-Cl and 9-Cl were the most abundant congeners in Northern Chile at Bewater (70%), Coloso (50%) and P. Milico (37%). A significant presence of low chlorinated congeners was detected in the extreme South of Chile. The sites of Punta Arenas I, II and III, showed a high congener composition dominated by 2-Cl, and accounted for 85%, 68% and 61%, respectively, of the total ∑PCB. The pattern was slightly different in Central Chile at Constitucion and Cocholgue where 3-Cl was 84% and 59%, respectively. In the case of Playa Hippie and Zapallar, 6-Cl (%) accounted for 45% and 40%, respectively, and 7-Cl (%) was higher at Huanillo (41%). PCA analysis clearly reveals five location groups. In most of the cases, the groups are composed of geographic areas close to each other, except for two sites: Papudo and Huanillo. This result is possibly due to the peculiar characteristics of both sites, since both sites present high anthropogenic uses. Also in general, the PCA results indicate that the sites located at higher latitudes present congeners with a smaller quantity of chlorines compared to those of lower latitudes (see Fig. 1, 2 and 3). To explore and to define more clearly the groups of sites with similar congeners, a hierarchical grouping analysis was performed, representing the multidimensional data graphically in a two-dimensional diagram. Fig. 4 presents the dendrogram by mean hierarchical group analysis where the formation of 5 groups is observed. This grouping fits well with the grouping detected by the PCA analysis. In the lower part of the figure, the group formed by Punta Arenas I, II and III are characterized as possessing congeners with a low chlorine substitution. Then, there is a group of three sites consisting of Lota, Constitucion and Cocholgue, where the last two are very similar. The sites of Northern Chile, Hippie, Zapallar and C. Huanillo, form a very similar group characterized by PCB congeners with 6-Cl and 7-Cl. The sites of Papudo, Huinay and C. Gonzalo possess very similar congeners (4-Cl) with Chaiten also being associated with this group. Finally, C. Coloso, Bewater and P. Milico form a quite compact group that had already been detected in the PCA analysis, and which is characterized by the congener presence of 5-Cl and 9-Cl. The PCA examined the variation and distribution the PCB congeners (from 2-Cl to 9-Cl congeners) in different com-

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Polychlorinated Biphenyls in Mussels

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(b)

(a)

Fig. 1: (a) Average ∑ PCBs concentrations (ng/g d.w.) and (b) congener distribution collected at each site

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Polychlorinated Biphenyls in Mussels

Table 2: Concentration of the PCB congeners in the different sampling regions (ng/g d.w.)

Congeners 15 18 31+28+50 44 49 54 60 77+154 86 87+61+116 101 114 118+149 121+88 128 129 138 141 143 151 153+105+127 159+182+187 170+190 171+202+156 173 180 183

C. Coloso

P. Milico

3.834

3.116

Bewater

Zapallar

Pappudo

Constitución

8.573 0.045 2.240

0.738 0.963

0.503

0.730 0.625

1.010

6.424 1.793

1.440

11.820 1.365

0.495

0.181 3.659 1.727 15.915

1.214 0.672 8.685 0.169

3.215 1.060 6.297 0.213

3.428 0.908

0.336

0.300

0.574

0.681

0.604

0.971

1.093

1.459

1.080

Cocholgue

4.611

8.046

C. Gonzalo

1.738 0.937

2.937

2.893 0.567 0.571 4.683 0.257

1.311 0.205 2.566

0.072 3.260 5.566 1.478 2.299 8.766 3.663 3.222 0.388 5.463 7.617

1.507 3.680

Lota

1.366 1.300

0.396 0.447

Congeners 15 18 31+28+50 44 49 54 60 77+154 86 87+61+116 101 114 118+149 121+88 128 129 138 141 143 151 153+105+127 159+182+187 170+190 171+202+156 173 180 183

Sampling sites Conc. ng/g d.w. P. H. Norte C. Huanillo

Sampling sites (Conc. ng/g d.w.) Chaiten Huinay Pta. Arenas I 111.318

2.640

5.014

0.616

0.192

2.628

Pta. Arenas II Pta. Arenas III 110.981 184.137 49.611 39.085

1.870 1.330

0.579

1.710 0.888 0.505 1.859

1.399

6.840

3.680

2.120

3.880 0.990 2.140 4.500

1.070 3.690

13.751

0.339

74.631

0.288

0.680

3.330

1.156 2.610

0.734 3.147 1.161

1.710 1.540 0.582

0.503 0.410

1.378

0.570 4.060

0.206 0.198

ESPR – Environ Sci & Pollut Res 13 (1) 2006

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Polychlorinated Biphenyls in Mussels

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1.0 5-cl

Factor 2 : 21.6%

9-cl

4-cl

0.5

0.0 8-cl

3-cl 2-cl

7-cl

-0.5 6-cl

-1.0 -1.0

-0.5

0.0

0.5

1.0

Factor 1 : 30.7%

Fig. 2: Principal Component Analysis (PCA) scores, distribution of PCB congeners (from 2-Cl to 9-Cl congeners)

3 C. Coloso 2

Huinay Bewater Papudo Caleta Gonzalo

Factor 2: 21.6%

1

Chaiten

P. Milico

Cocholgue

0

Constitución Pta. Arenas III

-1

C. Huanillo Lota

Pta. Arenas I

Playa Hippie Norte Zapallar

Pta. Arenas II -2

-3 -3

-2

-1

0

1

2

3

Factor 1: 30.7%

Fig. 3: Principal Component Analysis (PCA) loads in the different sampling sites

mercial formulations (Arochlor 1254, 1260, 1016, 1242, 1248; Clophen A30 and A60; Kanechlor 300, 400 and 500) (EPA 2000). Fig. 5 and Fig. 6 show the separation by percentage of the number of chlorines and commercial formulations characterized by presenting a certain number of chlorines. Arochlor 1260 presents greater proportions of 7Cl, 8-Cl and 9-Cl, and Arochlor 1254 greater proportions of 5-Cl. These results agree with the data on the % of chlo-

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rine in the sites of North, North-Central and South-Central Chile, being those used in Chile as long as Clophen A30, Kanechlor 300 and Arochlor 1016 which are characterized as possessing 2-Cl and 3-Cl, the characteristic profile of the Pta. Arenas area. Consequently, it is possible then to infer that these PCBs probably arrived by long range transport to those latitudes since record of their use in that area does not exist (CONAMA 2005, in press).

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Polychlorinated Biphenyls in Mussels

Kanechlor 500

C. Coloso

1.5

Arochlor 1254

Bewater P. Milico Papudo Huinay

1.0

Arochlor 1248

0.5

Kanechlor 400

Caleta Gonzalo

Factor 2: 26.6%

Chaiten Playa Hippie Norte Zapallar C. Huanillo Constitución Cocholgue

Clophen A 60 0.0 Arochlor 1242

Lota

-0.5

Pta. Arenas I Pta. Arenas III

Clophen A30 Kanechlor 300

Pta. Arenas II

-1.0 0

20

40

60

80

100

Arochlor 1260

120

Arochlor 1016

(Dlink/Dmax)*100

-1.5

Fig. 4: Hierarchical group analysis

-2.0

1.0

2.0

Fig. 5: Principal Component Analysis (PCA) scores, distribution of the PCB congeners (from 2-Cl to 9-Cl congeners)

5-cl

0.5 Factor 2 : 26.6%

0.0 Factor 1: 61.6%

1.0

Wania et al. 1998). This transport would mobilize such pollutants from low to high latitudes. This process of global fractionation causes a change in the relative PCB composition that could be reflected in the different environmental media.

4-cl

6-cl 0.0 7-cl

8-cl

9-cl

3-cl

-0.5 2-cl

-1.0 -1.0

-0.5

0.0

0.5

1.0

Factor 1 : 61.6%

Fig. 6: Principal Component Analysis (PCA) loads for different commercial formulations (Arochlor 1254, 1260, 1016, 1242, 1248; Clophen A30 and A60; Kanechlor 300, 400 and 500) 2.3

-1.0

Changes in PCB congeners composition along latitudinal gradient

Several authors have observed preferential accumulation of higher chlorinated PCB congeners in mytilids (Boon and Eijgenraam 1988, Colombo et al. 1995, 1997, Kammann et al. 1992), similar to our results obtained in North and NorthCentral Chile, and which is probably due to the metabolism of low chlorinated congeners (Thompson et al. 1999). Indeed, bivalves have a certain capacity to metabolize these organic contaminants (Livingstone 1994). However, as the latitude increases, the light congeners increase proportionally. In addition to biodegradation, other processes could be associated with the observed results, such as the atmospheric PCB input in such areas. After atmospheric release, PCBs could experience long range transport, where the octanolair partitioning coefficient and their temperature dependence have been used as descriptors of this effect (Bidleman 1988,

ESPR – Environ Sci & Pollut Res 13 (1) 2006

Recent results on PCBs levels in soils and lake sediments throughout Chile showed higher than expected PCB concentrations in remote areas of Southern Chile (Borghini et al. 2005). Indeed, depositional fluxes of these compounds were found to have increased significantly in the last 50 years, being higher in recent years (Barra et al. 2004a, b), presenting a trend that is reverse to the trend shown by data gathered in areas from the Northern hemisphere, where these products were banned from 1970s onward and the maximum depositional fluxes where observed in that period (Muir et al. 1995, 1996). Recent data on PCBs in air, obtained through passive samplers (3 weeks of deployment) in Punta Arenas (Pozo et al. 2004), shows very low levels of volatile congeners in that area, which contrasts with our results in bivalves. However, differences in sampling periods and strategies make a comparison very difficult. This result suggests the need to look at other potential PCB sources to explain the high PCB levels observed in the extreme South of Chile. 3

Conclusions

P. purpuratus was shown to be a good bioindicador of coastal PCB levels. Higher concentrations and more volatile congeners of PCBs were observed in the extreme South of Chile, where this result is explained as a long range transport process or as being due to illegal PCB discharges in that area (a maritime route of high relevance). Similar results – expressed as concentrations – were obtained 10 years ago by the International Mussel Watch Program, but using different species. Further studies are needed to understand the major

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Polychlorinated Biphenyls in Mussels source pathways of PCB entry into these areas. By using the congeneric distribution, a similitude pattern was observed with the commercial formula of Arochlor 1254 and Arochlor 1260 in Chile, with the exception of in the South and extreme South. Acknowledgements. This work was supported by FONDECYT-Chile Grant No. 1050647. This paper was written inspired in the ideas of Davide Calamari. We were fortunate to meet him and be influenced by his innovative scientific spirit, thanks Davide for your friendship. This work is part of a Doctoral Dissertation in Environmental Sciences of Gonzalo Mendoza, supervised by Ricardo Barra. Thanks are also given to the Graduate School of the University of Concepcion.

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ESPR – Environ Sci & Pollut Res 13 (1) 2006