Overview of the 20Th Century Impact of Trace Metal Contamination in The

Marine Pollution Bulletin xxx (2012) xxx–xxx

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Marine Pollution Bulletin

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Baseline Overview of the 20th century impact of trace metal contamination in the estuaries of Todos os Santos Bay: Past, present and future scenarios q ⇑ Vanessa Hatje a, , Francisco Barros b a Laboratório de Oceanograﬁa Química, Instituto de Química, UFBA, Campus Ondina, Salvador, BA 40170-290, Brazil b Laboratório de Ecologia Bentônica, Instituto de Biologia, UFBA, Ondina, Salvador, BA 40170-215, Brazil article info abstract

Keywords: This paper discusses the distribution patterns of trace metals in sediments and suspended particulate Subaé matter (SPM) in the three main estuaries of the Todos os Santos Bay (BTS), Brazil, during dry and rainy Paraguaçu seasons. Data available up to 2012 was also reviewed to assess the status of contamination. For most ele- Jaguaripe ments, metal concentrations in sediments decreased from the tidal limits to the lower estuary. Metals in Geochemistry SPM presented more complex distributions along the salinity gradient. Metal variability between rainy Review and dry conditions was only signiﬁcant for SPM data. Of the BTS estuaries, the levels of Cd, Zn, Pb and Metals Cu are highest in the Subaé estuary, and they seem to be promoting harmful biological effects in macrofauna, and also may pose potential human health risks. Despite the evidence of important localized contamination, much of the data compiled indicates that the bay and its estuaries are still relatively preserved. Ó 2012 Elsevier Ltd. All rights reserved.

The Todos os Santos Bay (BTS, Fig. 1) is located in the vicinity of Cavalo dam it has an average discharge of 64 m3 sÀ1 (Genz, the third biggest metropolitan area in Brazil, the city of Salvador. It 2006). Maximum flows are observed during the summer months, is the second largest bay of Brazil, with an area of 1112 km2 and especially in December and January. The other two main tributar- approximate maximum width and length of 32 km and 50 km, ies of the BTS are the Jaguaripe (2200 km2) and Subaé rivers respectively. The bay is relatively shallow (i.e. average depth of (600 km2). The maximum discharge of the Jaguaripe and Subaé 9.8 m) and presents an intertidal area of 327 km2. The geomorphol- rivers occurs in June (winter), where mean monthly discharges of ogy of the bay is determined by tectonic alignments. Deep drainage 28 m3 sÀ1 and 9 m3 sÀ1 are observed, respectively (Cirano and channels, reaching depths up to 70 m, ramify inside the bay follow- Lessa, 2007). ing an old drainage network going towards Paraguaçu River, Subaé The BTS is of a historical socio-economic importance. There was rivers and Aratu Bay (Cirano and Lessa, 2007). a profound change in the surroundings of the bay between 1501, The circulation inside the bay is mostly tidally driven. During when the Portuguese first entered the BTS, and 1590, when the summer, the waters inside the bay have oceanic characteristics, first urban complex on the edge of the bay, the city of Salvador, while during winter there is a significant increase in freshwater had became fully active. At that time, the Recôncavo Baiano region, fluxes. Tides are characteristically semi-diurnal, with a maximum which embraces the whole area of the BTS, was covered by dense range of 3.5 m during spring tides at Iguape Bay (Fig. 1), and rainforest and mangroves. From 1550, however, the cultivation of 1.2 m during neap tides at the main entrance to the BTS. In terms sugar cane, and subsequent developments leading to more com- of sediments, siliciclastic sand can be found in the channels at the plex business activities promoted a rapid destruction of the native entrance to the bay and close to the river mouths, whereas mud oc- vegetation. A significant change occurred in 1950, when a refinery curs predominantly in the northern part of the bay (Dias, 2004). was installed on the shore of the BTS, and led to the development The Paraguaçu, Subaé and Jaguaripe rivers (Fig. 1) are the three of the petrochemical industry. As a result of this process, there has main tributaries of the BTS. The catchment area of the Paraguaçu been extensive industrial development in the surroundings of the River measures 56,300 km2, and downstream of the Pedra do BTS, including the largest petrochemical complex in the southern hemisphere. In summary, several anthropogenic activities currently influ- q ‘‘Capsule’’: Recent data on metal geochemistry in the Paraguaçu, Jaguaripe and ence the environmental quality of the BTS, such as the influx of Subaé estuaries and existing information on metals in the Todos os Santos Bay, up domestic and industrial effluents, solid wastes, agriculture, ports to 2012, is compiled and reviewed. ⇑ Corresponding author. Tel./fax: +55 71 32355166. and mining activities (CRA, 2001, 2008; Hatje et al., 2009). Some- E-mail address: [email protected] (V. Hatje). what surprisingly, there have been few published articles of the

Fig. 1. Location of sampling stations in the Paraguaçu, Subaé and Jaguaripe estuaries, Todos os Santos Bay, Brazil. occurrence and effects of metals within the BTS and its tributaries. August, 2007) (Fig. 1). Surveys included the measurement of salin- Nevertheless, relatively high concentrations of trace elements and ity, dissolved oxygen, temperature and SPM, and water and sedi- hydrocarbons (HPAs) are observed in marine invertebrates ment collection from 10 or 11 stations along axial transects of (Wallner-Kersanach et al., 2000; CRA, 2004; Amado Filho et al., the main channel of each estuary (Fig. 1). The locations of the sta- 2004; Hatje et al., 2009), sediments (CRA, 2004; Venturini et al., tions were intended to provide representative estuarine gradient 2004, 2008; Barros et al., 2008; Hatje et al., 2006a, 2009, 2010), data. Physico-chemical variables were measured with a water and atmospheric particles (Pereira et al., 2007; da Rocha et al., quality analyzer (Datasonda Hydrolab 4A, Colorado, USA). At each 2009), especially in the northern region of the bay. site, water samples and sediments were collected in precleaned Although a lot of effort has been made to reduce metal point polyethylene bottles. Samples were collected by hand-dipping bot- sources emission, such as the strengthening of control policies, tles beneath the water surface. The bottles were capped immedi- very little has been achieved regarding non-point source emis- ately, sealed inside two polyethylene bags and transported to the sions. Untreated sewage is still a large problem, and therefore in laboratory. In the laboratory, samples were ﬁltered through a many regions contamination has possibly increased rather than pre-weighed 0.45 lm Millipore membrane (cellulose). The mem- decreased. branes with SPM were rinsed three times with 20 ml of ultrapure The aims of this study are to present and discuss the distribu- water to remove salt, dried and subsequently reweighed to obtain tion patterns and behavior of trace metals in sediments and SPM the mass of SPM. in the main estuaries of the BTS. This study also reviewed and com- Sediment samples from the Subaé and Jaguaripe rivers were piled the existing knowledge regarding trace metal contamination collected by SCUBA divers using a 5 cm diameter PVC core that in the BTS. The data regarding biota contamination was discussed was dragged, horizontally, for 2 m in surface sediments (1–5 cm). in de Souza et al. (2011). Once the sample was collected, the core was capped and the tube Campaigns, in both dry and rainy conditions, were carried out at retrieved. Sediment samples from the Paraguaçu estuary were col- Paraguaçu (May and December, 2005), Subaé (June, 2004; March, lected with a Van Veen dredge, and a portion of the superﬁcial 2006; December, 2009; April, 2011), and Jaguaripe (May, 2006; 5 cm sediments was scooped from the center of the dredge.

Samples were transferred to a pre-cleaned LDPE container and kept frozen until analysis. All bottles and materials used for the collection and analysis were cleaned and immersed for at least 24 h in extran detergent solution and for a further 48 h in a 10% HNO3 solution, rinsed with ultra pure water, dried on a clean covered bench and stored in zip-lock bags before use. Sediment samples were divided into two parts, the ﬁrst used for the determination of particle-size distribution, and the second for chemical analyses. Before chemical analyses, sediments were wet sieved to separate the fraction smaller than 63 lm, freeze-dried, homogenized and comminuted in a ball mill. An extraction using 20 ml of 1 M HCl, shaking for 12 h at room temperature, was carried out with sediments and SPM samples. Sediment and SPM samples were extracted in triplicates. Elements were determined using ICP OES (Varian, VISTA-PRO). Blanks were included in each batch of analysis. The precision and accuracy of the analytical technique were assessed using a CRM, MESS-2 (National Research Council of Canada) with each batch of samples. As expected, results indi- cated good analytical precision, but incomplete digestion (i.e. recovery varied from 1.5% to 63% for Al and Mn, respectively). All procedures including the sample collection and analyses were carefully undertaken in order to reduce potential contamination.

Organic Carbon (Corg), N and S were determinated by a LECO Elemental Analyser (Leco, TruSpec CNS). Sediments were freeze- dried, homogenized and comminuted in a ball mill. Prior to Corg determination, carbonate were removed using HCl, then the sediments were dried in an oven (100–105 °C) to constant weight and store in desiccators until analysis. Accuracy of element analysis was checked employing C, N and S Soil CRMs (Thermo Soil Ref- erence NCs, Italy and LECO Soil Calibration Sample, USA). Recovery for C, N and S varied from 92% to 104%. Person correlation coefficients were calculated to evaluate the specific relationship between two variables. Additionally, Principal component analyses (PCA) were performed, separately, with sediment and SPM data which were first normalized and log (x +1) transformed to account for the different units of the variables. The environmental conditions of the tributaries have already been described in detail elsewhere (Hatje et al., 2010). The estuarine waters are, in general, well-oxygenated and display low tur- bidity (Fig. 2). The salinity and the concentration of SPM varied between sampling dates due to seasonal changes in precipitation and fluvial influx of freshwater. In the Jaguaripe estuary, during the dry season, weather conditions at the catchment area were atypical, which resulted in anomalous physicochemical character- Fig. 2. Distribution of suspended particulate material in the Paraguaçu, Subaé and istics for this time of the year, as can be seen in Fig. 2. Maximum Jaguaripe estuaries. concentrations of SPM in the Subaé estuary (86.4 mg kgÀ1) were similar to those observed in the Jaguaripe estuary, nevertheless, it has been reported that the Subaé is the main source of SPM for in the Itapagipe Bay (Fig. 1), which is heavily contaminated by sew- the BTS (Hatje et al., 2006a; Cirano and Lessa, 2007). age. Domestic effluents, not only in the Itapagipe Bay, but for the Very few data, from secondary sources, is available for trace entire BTS system, are important sources of organic matter that metals in the water column, either for the tributaries or the main can act as an efficient ligand for Cu2+. However, most of the BTS BTS water body, as can be observed from the few theses and re- area showed that the Cu complexation capacity is low (8–28 nM; ports (Reis, 1975; CRA, 1996, 1998, 2004; Petrobras, 2003, 2005; CRA, 2004). This information added to the lack of correlation be- FUNDESPA, 2001; Queiroz, 1992; Bonfim, 2005), mostly with re- tween this data and the dissolved organic carbon, suggests that a stricted circulation, that have been published in the scientific liter- large part of dissolved organic material is not available for binding ature. This paucity of published studies on dissolved metal data is to Cu (CRA, 2004). surprising for such an important bay. Neither the use of ‘‘clean’’ For elements, such as Zn, Cu and Cd the bioavailable and poten- techniques nor the use of CRMs were reported in most of these tially most toxic species are the free ions. There is a wide discrep- studies. Moreover, most of the data corresponds to the fluvial ancy in the very few dissolved trace metal concentrations areas, especially the Subaé River, or to the main BTS water body, reported for the BTS. For instance, Bonfim (2005) reported values and there are no available background levels for the BTS waters. of 130 ± 4 mg LÀ1 and 23 ± 2 mg LÀ1 for Zn and Cu, respectively, in It is well known that most dissolved trace metals are present as the northwest area of the BTS, while CRA (2004) found 4.19 mg LÀ1 organic complex in marine waters. This is the case of Cu, the organ- and 1.01 mg LÀ1, respectively, for the same region. The comparison ic complexation of which can represent up to 100% of the total dis- of scientifically sound results for the BTS (i.e. data with QA/QC; CRA, solved metal (Donat and Bruland, 1995; Bruland and Lohan, 2003). 2004) and data for the Guanabara Bay (Alevato et al., 1981; Rebelo CRA (2004) reported the highest Cu complexation capacity (67 nM) et al., 1986; Rangel et al., 2011), the Thames estuary (Popo and

Langston, 2011), and the Port Jackson estuary (Hatje et al., 2003a), Maragogipinho, there is also a traditional production of handmade which are well documented degraded areas, suggests that Cu and ceramic pots and pans, and the paint used in this process is a Zn concentrations, especially at the Aratu Bay and the mouth of source of metals, including Cu, Cd and Pb. the Subaé estuary, are high and deserve to be further investigated. Another pattern observed in the trace metal profiles was the in- Based on the scarce and also sometimes conflicting results for crease in trace metal concentrations towards the estuary mouth, i.e. trace metal concentrations in the water column, it is important an increase in metal concentrations accompanying an increase in to highlight the need to produce more scientifically sound data salinity and pH. This pattern, with the highest concentrations for both the BTS and its tributaries, especially, because these are observed within the salinity range of 20–30, occurred mainly in fundamental to ascertain the bioavailability and toxicity of dis- during dry conditions, when the salt water intrusion reached the solved metals to marine biota. upper parts of the estuaries, so the freshwater influence, and the The chemical composition and variability of SPM in estuaries low salinity zone, was restricted to a small area. It is well know that and bays is controlled by a complex interplay of physical and bio- salinity affects the distribution of solid-dissolved species of trace geochemical processes. Some of the most important geochemical metals through the competitive, complexing and electro-strictive processes influencing variability are the mixing of riverine sus- effects of ionic strength (Turner and Rawling, 2001; Turner et al., pended matter with marine material (Verlan et al., 1998; Turner 2002). For Pb at Jaguaripe and Paraguaçu, for Ni at Paraguaçu and et al., 1991), flocculation of colloidal material (Benoit et al., Subaé, for Zn and Cr at Jaguaripe and for Mn at Jaguaripe in not only 1994), adsorption and desorption in low salinity zones (Windom dry but also during rainy conditions, trace metal concentrations et al., 1988; Zwolsman et al., 1997), production of organic matter increased seawards. Depending on the element, a more or less by phytoplankton (Balls, 1990; Burton et al., 1994), suspended par- pronounced increase in the concentrations, possibly in the Fe-Mn ticulate matter content and resuspension of bottom sediments oxide phase, is the result of the sorption of trace metals onto bind- (Hatje et al., 2001a, 2001b, Hatje et al., 2003b). In general, the ing sites on the particle surfaces, caused by a rise in pH. It has been behavior of trace metals in estuarine waters is extremely variable, shown that a small shift in pH can produce a sharp increase in and few dominant patterns can be observed in the literature. particulate metal concentrations (Hamilton-Taylor et al., 1997; Axial transects of trace metals in SPM, from each campaign at Lead et al., 1999; Hatje et al., 2003b), and further, that Pb and Cu each estuary, are given in Fig. 3. For the estuaries studied no clear are more strongly bound to oxy-hydroxide surfaces than other trace pattern could be identified for many of the elements other than metals (e.g. Ni and Zn; Forstner, 1987). that the highest metals concentration (i.e. Cd, Co, Cu, Mn, Pb and Of the metals studied, Cd was the only element that presented Zn) occurred in the Subaé estuary. The high level of SPM contami- concentrations below detection limits (0.002 mg kgÀ1) in the nation by metals in the Subaé estuary derives from the large waste Jaguaripe and Paraguaçu estuaries in rainy conditions. Moreover, reservoir of a lead smelter which was decommissioned in 1993. no clear pattern could be observed for Cd at Paraguaçu under dry The Pb smelter produced 11–32 Â 106 kg of Pb bars yearÀ1.Itis conditions as shown in Fig. 3. estimated that, during its operation, more than 25 Â 107 kg of Cd Although the number of field campaigns undertaken was not were discharged into the river, at least another 15 Â 107 kg have high enough to test temporal variation, the results showed a signif- been released in the atmosphere, whereas the lead burden is diffi- icant difference between dry and rainy conditions for most ele- cult to estimate (Hatje et al., 2006b). ments, suggesting that metal concentrations in SPM may be In general, the axial profiles of Pb, Zn, Cu and Cd, in SPM from controlled by seasonal changes in freshwater discharge. In the case the Subaé estuary, both during the dry and rainy seasons, showed of the Subaé estuary, the concentrations of Ni, Co, Mn, Cr, Cu and a decrease in metal concentrations towards the estuary mouth. Zn were significantly higher during the rainy season, i.e. when This clearly reflects the dilution effect on the contaminated SPM the waste reservoir and the deposition lagoons of the decommis- from the fluvial system, in the vicinities of the Pb smelter, with sioned Pb smelter are washed by rain water. In this case, a mobili- the SPM from the BTS ‘‘marine’’ end member. The lead smelter is zation of large amounts of contaminants is expected, added to the not the only source of contamination for this system. Paper and runoff inputs from urban and rural areas. In the Jaguaripe estuary food industries, a few villages and, especially, several point sources the highest concentrations of Mn and Ni were also observed during of untreated sewage discharge can also be found all along the estu- the rainy season. On the other hand, for the Paraguaçu estuary the ary, contributing to the metal contamination. highest concentrations of Ni, Mn and Cu occurred during the dry The greatest factors determining the chemical dynamics of season. The Paraguaçu basin is quite particular, in the sense that suspended matter are the concentration and composition of it is a very large basin that crosses regions with different climates suspended matter and the salinity gradient (Turner et al., 1994). (semi-arid to coastal) which might produce patterns that are more As can be seen in Fig. 3, the profiles of Mn and Co under rainy complex. Additionally, the upper part of the Paraguaçu River is and dry conditions and also Zn and Cu during the rainy season dammed, which reduces the natural flow variation, buffering the presented a peak in the upper estuary (between sites 6 and 8). seasonal effect expected on metal and SPM concentrations. Only Nevertheless, only Mn presented significant relationship with Zn and Pb presented higher concentrations in rainy conditions. SPM (r = 0.51, p < 0.05). For the other elements, such as Co and These are possibly associated with sewage inputs downstream Zn, no significant relationship was observed between SPM concen- from the dam, and therefore presented high concentrations during trations and the metals in Subaé estuary (r = 0.41 and 0.12, high flows. p > 0.05, for Co and Zn respectively), suggesting that an important The Principal Component Analysis (PCA) for the SPM explained local source could be present in this area, other than the resuspen- 71.2% of the total data variability (Fig. 4). The PC1 corresponded to sion of sediments, caused from wind-driven and tidal action, that 36.6% of the total data variability and distinguished the data from may mobilize trace metals stored in the sediments of microtidal the Subaé estuary, which is highly impacted by anthropogenic estuaries (Hatje et al., 2006a; Hatje, 2003). sources of trace metals, from the other two estuaries. Copper, Zn, The spatial pattern of decreasing concentrations towards the Pb, Co and Cd presented strong negative correlation with PC1. estuary mouth was observed for Co and Cu in Jaguaripe, during Thus, this PC can be used to illustrate the contamination gradient the dry and rainy seasons. This was also observed for Cu in along the BTS estuaries. The PC2 represented 19.3% of the total var- Paraguaçu under low flow conditions. There are small settlements iability. This PC corresponded to the physicochemical characteris- at the heads of Jaguaripe and Paraguaçu estuaries which discharge tics of the water. Salinity, pH and Ni were strongly correlated to untreated sewage in the water. At Jaguaripe, especially at PC2, whereas SPM was negatively correlated. This PC separated

Fig. 3. Axial proﬁles of metal concentrations in suspended particulate material in the Paraguaçu, Subaé and Jaguaripe estuaries.

(p > 0.05) between C and N levels in sediments collected during the rainy and dry seasons for the estuaries studied. The highest val-

ues of Corg and N were observed in the Jaguaripe estuary, where exuberant mangroves can be found on most of the estuarine shore. Anthropogenic influences, in this latter system, are limited and it is thought to have a relatively small impact on the environmental quality, especially when compared to other estuaries. Ratios of C/ N have been used to ascribe the origin of the organic matter (Saito et al., 1989; Stein, 1991; Cifuentes et al., 1996). Although there are some differences in the literature, C/N ratios lower than 10 are usually attributed to organic matter from a marine source, whereas ratios above 10 suggest a mixture of terrestrial and marine organic compounds in sediments. The Subaé and Paraguaçu estuaries presented C/N ratios (Table 1) that indicate a marine source for the organic matter present in the sediments, despite the high input of organic material from untreated sewage. The Jaguaripe estuary, however, presented not only organic matter from marine sources, but also a terrestrial signal, likely to be associated with the extensive mangrove located all around the estuary. Data for S and C/S ratios are also presented in Table 1. The C/S ratios varied from 1.12 to 7.42, from 0.89 to 7.52 and from 0.88 to 4.15, respectively for the Jaguaripe, Paraguaçu and Subaé estuar- Fig. 4. Principal component analyses performed on metal concentrations in SPM in ies. These values, when compared to the work of Leventhal (1983) the Subaé (Sub), Jaguaripe (Jag) and Paraguaçu (Par) estuaries. and Berner (1989), can be used to classify the environment in oxygenated or anoxic. According to these authors, sediments with C/S ratios below 2.8 indicate sediments tending to anoxic conditions. the data from the Paraguaçu and Jaguaripe estuaries. Based on More than 50% of the superficial sediments from the Subaé pre- these results it can be seen that toxic metals associated to SPM sented, in both, dry and rainy seasons C/S ratios below or close and physicochemical variables define different geochemical envi- to 2.8. Subaé results, in those stations, had similar levels to those ronments in the three studied estuaries. obtained from cores collected at the mouth of the estuary, which For the sediments, the main grain size of the estuaries is sand, present anoxic conditions at the bottom (Costa et al., 2011). In as has been discussed elsewhere (Hatje et al., 2010). In the Jagua- the Jaguaripe and Paraguaçu estuaries only around 30% of the sed- ripe estuary, the granulometry of the entire estuary was relatively iments presented C/S ratios close to or below 2.8. uniform, during both the dry and rainy seasons, and more than 90% Most of the metal studies carried out on sediments from the BTS of the sediment had grain sizes between >64 lm and <2 mm. The are descriptive and used regular grids to sample areas more prone Paraguaçu and Subaé estuaries presented similar grain size distri- to environmental impacts, i.e. the regions adjacent to heavily butions, whereas the majority of upstream sites were dominated industrialized areas in the northeast part of the bay. The estuaries by sand, fine particles represented a significant portion of down- have been neglected to date. Compared to water and SPM compart- stream sediments, close to the mouths of the estuaries. Siliciclastic ments, the number of studies on the sediments of the BTS system is sand occurs in the channels at the entrance to the main BTS area, much higher. Published results on metal contamination in sedi- along the western margin of the bay and close to the river mouths ments date from the seventies (Brandão and Tavares, 1978; Freire (Cirano and Lessa, 2007). Mud occurs predominantly in the north- Filho, 1979). Among these, two studies established the trace ele- ern half of the bay due to the drainage of fine grained sedimentary ment background values for the bay (Table 2). In these studies, da- rocks. Gravel is often observed in the fluvial delta of the Paraguaçu ted sediment profiles were used to determine the natural levels of estuary (Cirano and Lessa, 2007). metals in the BTS. The organic matter content, which is usually associated with the The trace metal concentrations for the most toxic elements, grain size of sediments, is very variable. The highest contents (3–6%) measured to date are compiled in Table 3. Most of the trace ele- are associated with fine sediments within the bay and the estuarine ments listed in this table were determined by atomic absorption (Dominguez and Bittencourt, 2009) and mangrove areas (8.2 ± 11%). spectrometry (AAS) and optical emission spectrometry using plas- Concentrations of organic carbon (Corg) in cores collected at the ma (ICP OES). The reported results in Table 3 correspond to analy- mouth of the Subaé estuary and in Mataripe (Fig. 1) showed a signif- ses of sediments with different granulometry; i.e. sediments icant decrease in the concentrations with depth (CRA, 2004). This 663 lm, which present a high adsorptive capacity, and sediments pattern suggests the mineralization of the organic matter in the sed- that did not undergo grain-size separation, although it has been iments and a possible change of the sedimentation regime due to the mentioned that granulometry in the area is quite variable (Cirano impact of industrial activities, which are important in these two and Lessa, 2007; Dominguez and Bittencourt, 2009). Many of the areas (CRA, 2004; Costa, 2006). Nitrogen contents obtained from studies reported in Table 3 did not present QA/QC results; and only core profiles in the northern part of the BTS range from 0.10% to the most recent studies presented CRM recoveries (e.g. CRA, 2004; 0.34%, and also decrease from top to bottom (CRA, 2004; Costa Hatje et al., 2006a, 2006b; Barros et al., 2008; Hatje et al., 2010). A et al., 2011). In general the highest values of Corg occurred at the factor that jeopardized long term temporal analysis was the large mouth of the Subaé estuary, and in the Itapagipe and Aratu Bays, diversity in the digestions and/or extraction of trace metals which and were correlated to N, suggesting that the N present in the sedi- ranged from diluted cold HCl extractions (Hatje et al., 2006a, ments is associated to the organic matter (Hatje et al., 2009). 2006b, 2010; Barros et al., 2008) to total digestion with HF and The Corg and N data for the Subaé, Paraguaçu and Jaguaripe estu- other concentrated mineral acids (Petrobras, 2003, 2005). The total aries are presented in Table 1. Concentrations for tributaries were digestions used in some studies (e.g. Petrobras, 2003) solubilized in the same range observed for the bay (i.e. 0.21–0.61 N% and 0.63– metals associated with silicates and primary minerals, in relatively 5.71 C%; Hatje et al., 2009). There were no significant differences stables phases in the sediments, as well as contaminants which are

Table 1

Concentrations of Corg%, N%, S% and C ratios for sediments in the main tributaries of the BTS.

N% Corg% C/N S% C/S Jaguaripe rainy 0.36–0.61 3.34–5.71 7.31–12.0 0. 89–3.17 1.80–4.53 Jaguaripe dry 0.30–0.51 3.25–5.86 7.17–13.3 0.49–4.36 1.12–7.42 Paraguaçu rainy 0.22–0.34 2.25–3.08 8,64–10.5 0.40–1.41 1.94–7.52 Paraguaçu dry 0.23–0.37 2.09–3.34 8.85–10.4 0.10–0.78 0.89–5.37 Subaé rainy 0.24–0.33 1.23–2.19 5,09–7.60 0,34–1.68 0.88–4.15 Subaé dry 0.21–0.35 0.63–2.24 3.08–6.37 0.41–1.21 0.99–3.86

Table 2 Background values (mg kgÀ1) for the BTS sediments.

Mn Cr Cu Zn Cd Pb As Hg* Co Ni References 344 ± 105 42.4 ± 8.7 16.4 ± 5.6 70.6 ± 1.5 0.03 ± 0.01 18.4 ± 8.0 5.0 a 17 617 Nd Nd CRA (2004) Nd 106 ± 9.0 23.0 ± 5.2 71.3 ± 8.8 0.08 ± 0.01 27.4 ± 8.8 Nd Nd 17.6 ± 1.2 33.3 ± 2.8 Argollo (2001)

Nd = not determined. * Concentration in lg/kg.

Table 3 Minimum and maximum concentration (mg kgÀ1) for selected trace metals in the BTS system.

Zn Pb Cu Cd As Ni Mn Cr References Min Max Min Max Min Max Min Max Min Max Min Max Min Max Min Max 20.1 58.4 10.7 34.5 4.25 15.2 0.034 0.281 0.80 8.05 5.64 19.6 151 1594 8.27 13.0 Paraguaçu estuary 37.2 667 10.9 325 10.4 33.7 0.20 3.48 2.25 13.2 5.83 23.7 54.4 410 5.58 9.45 Subaé estuary 26.7 71.1 11.0 27.8 2.52 20.4 0.001 0.449 1.39 26.3 1.48 11.4 111 2109 6.25 17.7 Jaguaripe estuary 72.2 320 25.0 148 37.0 96.0 3.40 3.40 – – – – – – – – CRA (2000) 4.00 1646 2.00 780 3.00 666 0.650 3.00 – – – – – – – – CRA (1996) 2.20 774 2.00 359 1.90 404 – – – – – – – – – – CRA (1997) 3.20 307 6.40 43.4 2.30 425 – – – – – – – – – – CRA (1998) 0.44 332 0.16 107 0.16 489 0.003 5.56

Fig. 5. Axial proﬁles of metal concentrations in sediments in the Paraguaçu, Subaé and Jaguaripe estuaries.

Please cite this article in press as: Hatje, V., Barros, F. Overview of the 20th century impact of trace metal contamination in the estuaries of Todos os Santos Bay: Past, present and future scenarios. Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.07.009 V. Hatje, F. Barros / Marine Pollution Bulletin xxx (2012) xxx–xxx 9 dry and rainy seasons, Jaguaripe during the dry season and Parag- Concentrations of trace metals in sediments and accessory data uaçu during the rainy season and for Co in the Subaé and Jagua- were combined for the Principal Component Analysis. The first two ripe estuaries in dry and rainy conditions (Fig. 5). Gradients were PCs explained 51.6% of the total variability, where PC1 and PC2 ac- steepest for the Subaé estuary, especially for Cd, Zn, Pb and Cu, counted for 33.4% and 18.2% of the variability, respectively (Fig. 6). the origin of which is associated with the decommissioned Pb Zinc, Pb, Ni, Cu, Cd elements, were the variables that presented neg- smelter (Brandão and Tavares, 1978; Hatje et al., 2006a). The high ative correlations with PC1. As such, this PC represents a gradient of levels of these contaminants in the upper Subaé estuary and flu- the degree of contamination of the sediments. In the ‘‘least contam- vial area seems to be promoting harmful biological effects in inated’’ side of this PC is located all of the stations from Jaguaripe macrofauna (Hatje et al., 2006a). Moreover, it has also been found estuary, regardless of the seasonal conditions at the time of sam- that the human population from Subaé catchment area, especially pling. On the other side, the most contaminated sites, i.e. all the sta- children, was heavily contaminated (Carvalho et al., 1984, 1985, tions in the Subaé estuary, can be observed. Most of the Paraguaçu 1989, 2003) by exposure to contaminated water, food and atmo- estuary stations are located on the left side of the PC, in the ‘‘less spheric particulate material (CRA, 2004, 2005; Santos, 2009; contaminated zone’’. However, due to the Co concentrations at a Souza et al., 2011). The highest concentrations in the upper couple of stations in the Paraguaçu estuary, a good separation be- Jaguaripe and Paraguaçu estuaries are due to the greater urbani- tween the Paraguaçu and Subaé data was not observed, as can be zation of these areas. In the case of Paraguaçu few industries and seen in Fig. 4, for the SPM data. The occurrence of these relatively private marinas also contribute to the anthropogenic signal in high concentrations of Co is yet to be investigated. Organic carbon, metal concentrations. N and S were the variables making up the PC2. The comparatively In general, particle reactive, geogenic elements, such as Mn and high concentrations of Corg, N and S, possibly reflect the influence Cr presented an increase in concentration seawards through the of the extensive mangrove areas exporting organic matter to the estuary (Fig. 5); in the case of Cr, following the same pattern ob- estuaries. The importance of the mangroves as a source of C, N served for SPM. and S, seems to be the reason to separate Jaguaripe from Paraguaçu There were no significant differences between the data col- estuary in the Fig. 6. Possible due to the ‘‘normalization’’ of the sed- lected under rainy and dry conditions. Based on metal concentra- iments prior to chemical analysis (due to sieving) with respect to tions in sediments it seems that weather conditions, i.e. the dry the grain size, sediment granulometry, together with the geogenic and rainy seasons, which influence water flow and sediment trans- elements such us Cr and Mn were not important in determining port through the system, do not have an important influence on the data clustering. The PCA did not distinguish between data from distribution pattern of trace metals in sediments in the BTS estuar- the rainy and dry seasons. ies. It is important to highlight that each studied system was sam- Loads and sources of metals together with the transport and pled during different seasons, so the data presented here reworking of sediments as well as physicochemical factors to- represents dry and rainy conditions from different years. This gether determined the distribution of metals in the estuarine sed- means that for long term monitoring of the metals studied in sediments and also likely in the infralittoral of the bay. The presence of iments, the season (dry or rainy condition) for sample collection a multiplicity of anthropogenic sources of metals in the basin re- should not be a major concern, if one is interested in following sults in a mosaic of hot spots for contaminants in the sediments, temporal variation in metal distribution profiles. not only in the estuaries themselves but also in the central BTS Concentrations of Cd, Cu, Ni, Pb and Zn exceeded Threshold Ef- area. Enrichment factors for the BTS sediments have been reported fect Levels (TEL; NOAA, 2008), from sediment quality guidelines, to be as high as 23, 41, 42 and 426, respectively for Zn, Cu, Pb and over much of the Subaé estuary. Zinc and Pb levels at two stations Cd (Hatje et al., 2009). The highest enrichment factor was observed in the upper estuary also exceeded Probably Effects Levels (PEL; for Cd at Mataripe, close to a refinery area, and in the Aratu and Ita- NOAA, 2008) from quality guidelines in all four field campaigns. pagipe Bays (Fig. 1), were a variety of chemical and petrochemical These findings suggest that these contaminants could be having adverse effects on biota across much of the Subaé estuary, as previously described by Hatje et al. (2006a). The correlated trends observed for Pb, Cd, Cu and Zn distributions are explained by the fact that the metals mentioned were impurities present in the ore used in the Pb smelter. Arsenic concentrations (Hatje et al., 2010)at more than 50% of the stations in the Jaguaripe estuary and few stations in the Paraguaçu and Subaé estuaries were above the TEL va- lue (i.e. 7.24 mg/kg), so the sediments of these estuaries may be toxic to sensitive benthic species. According to Hatje et al. (2010) As (V) was the dominant species in the Subaé and Paraguaçu estuaries, which is less toxic and less mobile than As (III). Nevertheless, in the Jaguaripe estuary, As (III) was the dominant species. In this study, however, it has been shown that the As in the sediments of the Jaguaripe estuary and at least part of the As in the Paraguaçu estuary is derived from a natural source, and the fate of this element may be linked to the stability of Fe3+ hydroxides. Cobalt and Mn concentrations do not have TEL and PEL values, only an Apparent Effects Threshold (AET). In the case of Mn, around 50% of the stations exceeded AET values, but since Mn background values for the basin are high (i.e. 344 ± 15; Table 2), adverse effects on biota due the Mn concentrations are not expected, at least for the main BTS tributaries. High concentrations of Mn, due to anthropogenic activities, have been observed in the Aratu and Igu- ape Bays (Mestrinho, 1998; Santos, 2002; CRA, 2004), and deserve Fig. 6. Principal component analyses performed on metal concentrations in attention. sediments in the Subaé (Sub), Jaguaripe (Jag) and Paraguaçu (Par) estuaries.

Please cite this article in press as: Hatje, V., Barros, F. Overview of the 20th century impact of trace metal contamination in the estuaries of Todos os Santos Bay: Past, present and future scenarios. Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.07.009 10 V. Hatje, F. Barros / Marine Pollution Bulletin xxx (2012) xxx–xxx industries, sewage inputs and harbor activities contribute to the Sample digestions, in the compiled literature, have been elevated Cd concentrations (CRA, 2004). Copper, that also pre- achieved with a combination of acids and procedures. Therefore, sented high enrichment, is a regional contamination problem for it would be advantageous to standardize extractions/digestions the BTS, mainly due to the high load of untreated sewage input to produce comparable data. Furthermore, only a minority of the from the margins of the BTS. Levels of Cu in the sediments of the studied employed CRMs to check the accuracy of the analytical Aratu harbor/Bay, Itapagipe Bay and in a harbor in the Paraguaçu procedure. The present study also points to the need for a long- estuary (Terminal São Roque) exceeded PEL values, suggesting term monitoring program, as data on contamination has remained the potential occurrence of adverse effects on biota (CRA, 2004; scarce. This program must include a standardization of analytical Hatje et al., 2009). procedures and the use of CRMs in order to compare results within Available data on metal concentrations in the main estuaries of the scientific community and to allow for data comparability over the BTS is limited and based on sediments, SPM and biota (Souza time, which would subsidize the characterization of changes due to et al., 2011). Trends in trace metal distributions in sediments along poor enforcements and/or the introduction of new activities in the the Paraguaçu, Subaé and Jaguaripe estuaries are consistent, gener- area. ally, decreasing in concentrations seawards from tidal limits. Metal Insufficient knowledge regarding environmental pollution in variability in sediments between rainy and dry conditions was not the BTS probably also hinders the development of effective ecosys- significant. Concentrations and distribution patterns of metals in tem management. Based on the results of this study and the data SPM is very variable within and between estuaries. Moreover, from the literature presented here, future research needs to in- weather conditions significantly affected metal concentrations. clude: (i) monitoring of all matrices (i.e. biota, sediments, SPM Comparison of metal concentrations in SPM and sediments sug- and water); (ii) investigation of fluxes across sediment–water, gests that both derived from the same source. Reworking of sedi- water–atmosphere, and continent–ocean interfaces; (iii) carrying ments, physicochemical variables and current inputs are likely to out risk assessments to estimate potential impacts on biota and control the distribution patterns observed in each estuary. Unfor- humans; (iv) use of multiple lines of evidence to quantify the level tunately, there is no database which would allow for a comparative of impact on each ecosystem; and (v) evaluation of the bioavail- evaluation of historical trends. However, since the number of ability of contaminants. industrial and port activities, as well as, the sewage load entering the BTS system has increased in the past few years, despite regula- tory efforts, it is expected that the metal burden, not only in the Acknowledgments estuaries but also in the BTS main area, is still increasing. The estuaries studied present a clear gradient in terms of metal contamina- V. Hatje (304528/2010-2) and F. Barros (302642/2008-0) were tion. The Subaé estuary is by far the most impacted by trace metals, sponsored by CNPq-Brazil. This work was supported by FAPESB especially due to the decommissioned Pb smelter and the load of (CVN 0049/2008) and CNPq (479669/2007-4; 478265/2008-5). untreated sewage which the waters receive. On the contrary, We wish to thank all of the students who helped in the sample col- Jaguaripe presents relatively well preserved conditions, which lection and in the sample pre-treatment steps. can be observed from the metal concentrations in sediments and SPM and the extensive mangrove, which occupies most of the estu- References arine margins and is an important source of organic matter in the system. Furthermore, the granulometry of the sediments, mainly Alves, T.C.A., 2002. Caracterização geoquímica do substrato lamoso de zonas de sand, and the free communication with the sea do not favor the manguezal da baía de Aratu, Bahia. Dissertação de mestrado. Programa de Pós- accumulation of contaminants in this system. The Paraguaçu estu- Graduação em Geoquímica e Meio Ambiente. Universidade Federal da Bahia, Salvador. ary is also relatively well preserved, however some industrial Alevato, S.J., Acebal, S.A., Rebello, A.L., 1981. 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