Ecological risks of trace metals in Guanabara Bay, Rio de Janeiro, Brazil: An index analysis approach

Ecotoxicology and Environmental Safety 133 (2016) 306–315

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Ecological risks of trace metals in Guanabara Bay, Rio de Janeiro, Brazil: An index analysis approach Valquiria Maria de Carvalho Aguiar a,n, Michelle Nunes de Lima a, Rodrigo Coutinho Abuchacra b, Paula Ferreira Falheiro Abuchacra c, José Antônio Baptista Neto a, Heloísa Vargas Borges a, Vitor Calôr de Oliveira c a Universidade Federal Fluminense, Instituto de Geociências, Departamento de Geologia e Geofísica Marinha, Avenida General Milton Tavares de Souza, s/n, Niterói, 24210-346 RJ, Brazil b Universidade do Estado do Rio de Janeiro (FFP), Rua Dr. Francisco Portela, 1470 São Gonçalo, 24435-005 RJ, Brazil c Universidade Federal Fluminense, Instituto de Geociências, Departamento de Geografia, Avenida General Milton Tavares de Souza, s/n, Niterói, 24210-346 RJ, Brazil

art ic l e i nf o

a b s t r a c t

Article history: Received 24 April 2016 Received in revised form 8 July 2016 Accepted 11 July 2016

Total concentrations of Ni, Cr, Cu, Pb and Zn were determined in surface sediments from 30 stations in Guanabara Bay in 1999 and 2008. An approach using various environmental indices was used to assess contamination status of metals. This approach allowed the comparison with different coastal areas. Background Enrichment Index, Contamination index and Ecological Risk index (Pollution Load Index; Sediment Quality Guideline Quotient and Ecological Risk Index) were calculated for the metals. Results revealed a great load of organic matter and significant increases in Cu and Pb levels between 1999 and 2008. The concentrations of Cr and Zn were of great concern, surpassing the values of Probable Effect Level reference values. In spite of the differences of each index, results effectively revealed the striking contamination in Guanabara Bay concerning trace metals, and also suggested potential risk to local biota. The contamination of the northwest area was notably higher than the rest of the bay. In comparison with some other coastal bays around the world, Guanabara Bay stood out as a remarkably contaminated environment. & 2016 Elsevier Inc. All rights reserved.

Keywords: Guanabara Bay Sediments Trace metals Ecological index Pollution index

1. Introduction The need to evaluate sediment quality in coastal areas comes from the fact that they act as a geological record, integrating changes and conditions over a period of time. In turn, the importance of studying trace metals in sediments arises from their toxicity and persistence in the environment. Some metals are essential for the metabolism of phytoplankton, as cofactors of metalloenzimes and proteins (Cu, Zn, Co, Ni, Mn, Cd, Fe). A good example is Zn, which, at low concentrations acts as a limiting nutrient, however, the increase of its concentration interferes in the metabolism of other essential metals. Cu, for instance, competitively inhibits Zn uptake, and therefore the requirements for Zn are elevated at high concentrations of Cu. In turn, Zn competitively inhibits Mn uptake, and at low manganese environments, even low concentrations of zinc can interfere with Mn nutrition of the cells (Morel et al., 1991; Morel and Price, 2003). Human activities, n

Corresponding author. E-mail address: [email protected] (V.M. de Carvalho Aguiar).

http://dx.doi.org/10.1016/j.ecoenv.2016.07.012 0147-6513/& 2016 Elsevier Inc. All rights reserved.

however, have been altering the natural concentrations of these elements, as well as their biogeochemical cycles (Morel et al., 1991; Bielicka et al., 2005). Coastal areas in particular, are subjected to the impact caused by trace metals, due to vast urbanization around them. The contamination of bottom sediments, especially with trace metals, can have some serious deleterious effects for local biota, in particular benthic communities, including decrease of biodiversity and malformation of organisms (Jitar et al., 2015; Youssef, 2015). Besides bioaccumulation, trace metals suffer biotransference, which is the transfer of these elements from a food source to consumers (Barwick and Maher, 2003; Bastami et al., 2015; Kwok et al., 2014; Mendoza-Carranza et al., 2015; Pejman et al., 2015; Zhang et al., 2016). Estuaries are the most productive environments in the world, and are usually under constant anthropogenic pressure caused by surrounding industrial activities and growth of urban areas. Guanabara Bay is the most prominent coastal bay in Brazil and is notorious for the degradation of its waters and sediments (Kjerfve et al., 1997; Perin et al., 1997; Barbosa et al., 2004; Machado et al., 2004; Geraldes et al., 2006; Cordeiro et al., 2008; Borges et al., 2009; Aguiar et al., 2011). The industrial effluents in

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307

2. Materials and methods

year, seasonally influenced. The bay is surrounded by the cities of Rio de Janeiro, Niterói, São Gonçalo and Duque de Caxias, and its margins have been used as discharge sites of solid wastes by the habitants and also by the surrounding industries. The discharge of untreated domestic sewage lowers the concentrations of dissolved oxygen, and alters turbidity and pH, besides other effects that affect the maintenance of ideal conditions for the survival of local biota and consequently affect human health (Carreira et al., 2001). Besides the discharge of untreated domestic sewage, the main anthropogenic activities that contribute to the degradation process of Guanabara Bay are related to deforestation of mangrove forests, dredging and channel straightening (Godoy et al., 1998). Some of the main rivers contributing with the contamination of Guanabara Bay are Estrela, Sarapuí, Irajá and São João de Meriti (Fig. 1). Aside from the degraded rivers from the drainage basin, a recently abandoned air-open landfill site, Gramacho, contributes to the contamination of the bay with slurry containing trace metals, since it is located right at the edge of the northwest portion of Guanabara Bay (Fig. 1). This abandoned landfill site has a lagoon of slurry, and excessive precipitation sometimes makes it overflows, turning Guanabara Bay into the final destination of this material. The Cunha channel (Fig. 1) is an effective anthropogenic source to Guanabara bay, since it is very contaminated and discharges directly into Fundão channel towards the coast (Barbosa et al., 2004). Currently, more than 11 million habitants live in the metropolitan area of Rio de Janeiro, being responsible for the discharge of tons of raw sewage (Patchineelam and Baptista Neto, 2007). This area is also the second biggest industrial site of Brazil, with over 12,500 industries located around its drainage basin and a big harbor in the city of Rio de Janeiro (Bidone and Carvalho, 2003; Soares-Gomes et al., in press), representing 25% of organic pollution and more than 90% of toxic substances released into the bay (Barrocas et al., 1995; Perin et al., 1997). According to Catanzaro et al. (2004) granulometric distribution of Guanabara bay reflects the energy of tidal currents which are directly influenced by the morphology of the bottom and by the coastline. Guanabara Bay is covered by sediments varying from silt to very coarse sand. In the inner portion of the bay fine sediments predominate, responsible for approximately 63% of the granulometric composition, followed by 35% of silt and 2% of sand. This sector of the bay suffers from intense deposition process due to the reduction of current velocities (Quaresma, 1997). In the northwest sector there is predominance of silt, not only resulting from low energy conditions but also due to the occurrence of mangrove forests that act as a trap for this fraction of sediments (Catanzaro et al., 2004). The great amount of fine sediments in Guanabara Bay accumulates high contents of organic matter, with more elevated values in the west portion, around 7.05%. The accumulation of organic matter in sediments of Guanabara Bay are related to the morphology of its bottom, grain size, restricted water circulation and also to the great input of sewage discharge into this area (Catanzaro et al., 2004).

2.1. Study area

2.2. Sampling and analysis

Guanabara Bay is located in the state of Rio de Janeiro, southeast of Brazil, and is considered one of the most degraded coastal environments in this country (Kjerfve et al., 1997; Baptista Neto et al., 2000; Machado et al., 2004; Aguiar et al., 2011). In 2000, 1.3 million of liters of fuel oil, leaked from a refinery located in the city of Duque de Caxias and Ilha do Governador, and contaminated water, sediments and biota at Guanabara Bay. The drainage basin of Guanabara Bay has an area of 4080 km2, composed of 32 distinct fluvial sub-basins. Six rivers are responsible for 85% of fluvial input into Guanabara Bay, varying from 100 to 230 m3 s
1 per

The sampling of 30 stations at Guanabara Bay occurred in two distinct periods: 1999 and 2008 (Fig. 1), during the end of dry season. Bottom sediments were obtained with a stainless steel Van Veen grab, and samples were immediately stored in plastic vials previously decontaminated with Extran and rinsed with Milli-Q water and HNO310% (v/v). Sediment samples were frozen at
20 °C until the moment of analysis. At the laboratory, sediments were freeze-dried and aliquots were taken for the determination of total organic carbon (TOC) and sulfur (S), granulometric analysis and trace elements: Cu, Zn,

this area consist in a considerable source of pollution for the waters of the bay, being almost completely responsible for trace metals and other substances that end up accumulated in sediments (Lima, 2006). Guanabara Bay has been on a worldwide spot concerning its environmental conditions since the city of Rio de Janeiro has been chosen to host Olympic games, which will take place in 2016. Public concerns involve the degradation of its waters and the effects they can cause for people in direct contact with it, however, not much has been said about the quality of sediments, which are a fundamental part of this ecosystem, and interact effectively with the water column. Usually reference values for background are extracted from standard fossil shale (Turekian and Wedephol, 1961), nevertheless, the abundance of coarser particles can lower theses values below this average, being more adequate to use a regional background associated with the granulometric composition of the area (Ruiz, 2001). Environmental monitoring generates a large data set that can be difficult to interpret due to the complex nature of relationships between measured variables. The aggregation of complex technical data into environmental indices provides a result that can be transmitted to the public in a simpler manner and also enable comparisons among different study areas. Some applications of environmental indices are: (i) evaluation of monitoring programs; (ii) ranking environmentally degraded sites; (iii) investigation of temporal changes in environmental conditions. In the last decades several indices have been developed and became an important tool in the interpretation of sediment quality, allowing comparison among estuaries and coastal areas throughout the world (Caeiro et al., 2005). Indices can be divided into different categories such as; (i) Background Enrichment Indices, that compare contaminants results with different background or baseline values found in literature; (ii) Ecological Risk Indices, which compare the current results with sediment quality guidelines (SQG) and (iii) Contamination Index, which can simply aggregate metal concentrations or compare the contaminants with clean or polluted stations measured in the study area (Wilson and Jeffrey, 1987; Ruiz, 2001; Riba et al., 2002; Long and MacDonald, 1998; Caeiro et al., 2005). It is worth noticing that the aggregation methods used in each index is different. The purpose of this study is to assess the evolution of contamination of Guanabara Bay through the selection of different environmental indices, to aggregate trace metal contamination at bottom sediments and also investigate potential biological hazard. Although in trace metals studies the bioavailable fraction is more important than the total concentration of these elements, the overall increase of trace metals in Guanabara Bay, measures the anthropogenic pressure over this important economic area, completely neglected by the public authorities, something that is proving to be very detrimental in the long term.

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Fig. 1. Sampling stations at Guanabara Bay and main rivers of the drainage basin.

Ni, Cr and Pb. Granulometric analysis was performed through laser light scattering using a particle analyzer Malvern Series 2000, after elimination of organic matter, through loss on ignition (LOI), and calcium carbonate (CaCO3), with HCl 10% (v/v). TOC and S were measured using a Perkin Elmer CHNS/O Analyzer 2400, after elimination of CaCO3 of the samples. Acetanilide was used as reference standard material for the determination of TOC. The determination of S occurred only for the samples of the first campaign in 1999 due to technical issues. Freeze dried samples were sieved and trace metals were determined in the pelitic fraction (o0.063 mm). Approximately 0.1 g

of sample was extracted with a mixture of HCl, HF and HNO3 (USEPA 3051, 1997) at a microwave digestion system (Microwave 3000, Perkin Elmer) and samples were analyzed in an atomic absorption spectrophotometer Perkin Elmer AAS 3100. The reference standard material used to validate the trace metals determination was the estuarine sediment NIST 1646a. Statistical analysis was performed to test significant differences and evaluate the variance of the samples. Mann-Whitney test (p o0.05) and Principal Component analysis (PCA) were applied to s the data set with Statistica7.0 . Values of TEL (Threshold Effect Level) and PEL (Probable Effect Level) were used as guidelines to

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evaluate the concentrations of trace metals in sediments (MacDonald et al., 1996). Based on the dataset available for calculation, the indices chosen to be used in the present study were the ones which presented threshold values, making it possible to classify the pollution degree of the study area: (i) Background Enrichment Indices, (ii) Ecological Risk Indices and (iii) Contamination Indices. Among the Ecological Risk Indices three types were calculated: (i) Pollution Load Index (Wilson and Jeffrey, 1987); (ii) Mean Sediment Quality Guideline Quotient (Long and MacDonald, 1998) and (iii) Potential Ecological Risk Index (Riba et al., 2002). 2.3. Background Enrichment Index 2.3.1. New index of geoaccumulation-NIgeo (Ruiz, 2001) The NIgeo takes into account different background values according to sediment grain size distribution and was developed for Cr, Cu, Zn and Pb only. It is computed individually for each element in each station.

NIgeo = log2

Cn 1. 5xBn

309

mCd o1.5–null to very low contamination; 1.5 omCd o2–low contamination; 2 rmCd–moderate contamination; 4 rmCd o8– high contamination; 8 rmCd o16–very high contamination; 16 rmCd o 32–extremely high contamination; mCd Z32–ultra high contamination. 2.5. Ecological Risk Indices 2.5.1. Pollution Load Index–PLI (Wilson and Jeffrey, 1987) Considered a robust tool, PLI has been used in several estuaries in Europe and US (Wilson and Elkaim, 1991; Wilson, 2003). It aggregates the different contaminants into a single value, being individually calculated for each station, and also for the whole system.

⎛ C − B⎞ ⎟ PLI = anti log10⎜ 1− ⎝ T − B⎠

(

1/ n

)

Total PLI = PLI1,PLI2 … PLIn

B is the baseline value. T is the threshold, minimum concentration associated with degradation or changes in the quality of the estuarine system.

Cn is the concentration of the metal. Bn is the concentration of the metal n in unpolluted sediments according to a list of regional backgrounds for different grain sizes. In the case of the present study the background values used in the calculation of NIgeo were chosen from the results found by Baptista Neto et al. (2006) at Guanabara Bay.

For each place or station, the PLI calculation takes into account all the n contaminants and varies from 10–unpolluted to 0–highly polluted.

Results are classified as: NIgeo o1–Unpolluted; 1 oNIgeo o 2– Lightly polluted; 2 oNIgeo o3–moderately polluted; 3 oNIgeo o 4– Highly polluted; 4 oNIgeo o5–Very polluted; NIgeo 45–Very highly polluted.

2.5.2. Mean Sediment Quality Guideline Quotient-SQG-Q (Long and MacDonald, 1998) The SQG-Q mixes all the contaminants, and can include PHAs and PCBs. It is calculated individually for each station.

2.4. Contamination Index

SQG − Q =

n

2.4.1. Modified Degree of Contamination-mCd (Abrahim and Parker, 2008) Hakanson (1980) originally developed the Degree of Contamination (Cd) with a restriction that required at least five samples and only for eight contaminants, PCB, Hg, Cd, As, Cu, Pb and Cr. With the intention of eliminate the restriction, concerning the number of samples, Abrahim and Parker (2008), modified the Cd, and adapted it to only one sample measure. The index aggregates all contaminants into a single value. 8

Cd =

∑ C if i=1

C if =

Csi Cni i=n

mCd =

∑i = 1 C if n

Cd is the degree of contamination. n is the number of determined elements. i is the ith element. Csi is the metal measured concentration. Cni is the metal background concentration. Environments can be classified through mCd as follows:

PEL _Q =

∑i PEL _Q i n

[Contaminant ] PEL

PEL_Q is the probable effect level quotient. [Contaminant] is the concentration of the trace metal. PEL is the probable effect level for each contaminant. SQG-Q can be interpreted as: SQQ-Q r1–unimpacted; 0.1 oSQG-Q o1–moderate impact potential for observing adverse biological effect; SQG-Q Z1–highly impacted for observing adverse biological effects. 2.5.3. Potential Ecological Risk Index-ERF (Riba et al., 2002) ERF does not aggregate the different contaminants into one value; it is computed individually for each element in each station.

ERF =

Ci − CSQV CSQV

Ci is the total concentration of each metal i measured in the sediment. CSQV is the highest concentration of the trace metal non-associated with biological effects (chemical concentration associated with adverse effects). Results of ERF Z1 classify the environment as polluted.

310

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Fig. 2. Distribution of Cu, Pb and TOC at Guanabara Bay in 1999 and 2008.

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Fig. 3. Distribution of Ni, Cr and Zn at Guanabara Bay in 1999 and 2008.

311

312

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3. Results and discussion 3.1. Granulometry, TOC, S and total Ni, Cr, Zn, Cu and Pb The granulometric distribution of Guanabara Bay reflects the hydrodynamic variations in the different sectors of this coastal area. The north and northwest areas showed the predominance of fine sediments, over 99% of silt and clay. Only around the central and southwest portion of the bay, the predominance of sandy sediments was observed (S34, S35, S45, S48, S56). Concentrations of TOC determined in the first sampling, in 1999, reached high values varying from 0.36 to 7.05% (Fig. 2). Stations with TOCo1% were located in the central portion of the bay, with higher contents of sand. Despite the fact that low energy environments favor the accumulation of organic matter, the results of TOC revealed strong anthropogenic influence, since marine environments naturally present concentrations of organic matter around 0.5% (Libes, 2009). Sulfur contents in surface sediments varied between 0.04% and 6.36% in 1999. The C/S ratios calculated for 1999 data, revealed a very reducing environment (Borrego et al., 1998) with most values o2, in agreement with the high concentrations of TOC that are likely to consume dissolved oxygen during remineralization. The only station with C/S46, indicating tendency to oxidation, was S48 with more than 75% of sand in its granulometric composition. Results reinforced the frequent episodes of hypoxia related in bottom waters of Guanabara bay (Kjerfve et al., 1997; Aguiar et al., 2011; 2013), producing a reducing environment with very low contents of dissolved oxygen. In 2008, TOC varied between 1.8% and 8.2% (Fig. 2) with no significant differences (p¼0.08118) compared to the previous campaign. More than 50% of the sampled stations presented TOC values similar to the ones found in the previous campaign, however, the increase in organic carbon was observed in the northeast portion of the bay (Fig. 2), with TOC values between 6.5% and 8.1% (S1, S3, S11, S14, S16, S17). Indeed, this part of Guanabara Bay (Fig. 1) is also the final destination of waters from some very polluted water bodies around it, such as Caceribu and Guaxindiba rivers (Aguiar et al., 2011), and the growth of local population within 10 years may have contributed to the increase of organic matter. In a general way, results concerning trace metals revealed that the area of the bay with the highest concentrations of these elements was the northwest portion, whereas lowest values were found at the entrance of the bay. Although the northwest and northeast portions of the bay present a similar granulometric composition of bottom sediments, the effective increase of trace elements concentrations was only observed towards northwest. This pattern can be explained by the presence of several industries in the west margin of the bay, and also the fluvial contribution of some of the most contaminated rivers in this area. According to a previous study conducted by Baptista Neto et al. (2006), stations that present the highest concentrations for all metals studied were the ones closer to the harbor area of Rio de Janeiro. This region is characterized by an intense vehicular flux, loading terminals, industrial activity concerning steel, building materials, amongst others, and is subjected to spills and accidents that can contribute to the increase of trace elements in its surroundings. Among the 30 stations sampled in 2008 (Fig. 3), 21 presented increase in Ni concentrations compared to the results obtained in 1999, nevertheless, the differences of Ni concentrations between the two campaigns were not considered statistically significant (p ¼0.140015). Concentrations of Ni were above TEL for 83% and 93% of the samples in 1999 and 2008, respectively (Table 1). With the exception of S46, all the other stations, that presented small concentrations of Ni, had a great amount of sand in their granulometric composition (S34, S35, S45, S56). Some stations presented an increase in Ni concentrations over 300% (S35, S45, and S46) between sampling periods, nevertheless, the concentrations

Table 1 Minimum and maximum concentrations of Cr, Zn, Cu, Pb and Ni at Guanabara Bay in 1999 and 2008 in comparison with Threshold Effect Levels (TEL), Probable Effect Levels (PEL) and local background values. Cr mg/kg

MinMax 2008 MinMax %samples 4TEL 1999 2008 %samples 4PEL 1999 2009 Reference values foraTEL a Reference values for PEL b Local background for Guanabara Bay a b

1999

Zn

Cu

1.72–272 12–755 5–188

Pb

Ni

2–193

2–38

18–297

23–698 18–423 18–287 11–41

79 87 14 20 52.3 160 2

86 80 25 36 124 271 5

93 100 11 30 18.7 108 3

76 93 3 20 30.2 112 2

83 93 93 – 15.9 42.8 1

MacDonald et al. (1996). Baptista Neto et al. (2006).

of this element remained under TEL. Anthropogenic sources of Ni include fertilizers, steel works, fuel combustion and metal plating and coating. The region of Guanabara Bay where extreme Ni enrichment was observed was the one around the harbor (Fig. 3), which could justify these results. Cr concentrations varied between 1.72 and 272 mg/kg in 1999 and from 18 to 297 mg/kg in 2008 (Table 1). Differences in the concentrations of Cr between both campaigns (Fig. 3) were not considered significant (p¼0.323107). Over 70% of the samples in 1999 presented Cr concentrations above TEL, and 14% above PEL. In 2008 the samples that exceeded TEL for Cr were 87%, and the percentage of samples above PEL reached 20%. Raises of Cr concentrations over 100% were observed at some stations (S28, S34, S35, S53, S56). The northwest portion of the bay concentrated most of the stations with Cr concentrations above PEL during both campaigns (S21, S23, S88, S90, S92). Sources of chromium are diverse, but mainly, the industrial use of this element is in the manufacturing of ferrous alloys and electroplating processes due to its resistance to corrosion, therefore, it is abundantly used in industry. Besides industrial effluents that reach the bay, the atmospheric transport is a major pathway for long range transport of Cr containing particles (Bielicka et al., 2005). Of the 30 stations sampled, 21 presented increases in Zn concentrations between 1999 and 2008 (Fig. 3), however, differences in concentrations between sampling periods were not considered significant (p ¼ 0.732101). Concentrations of Zn varied between 12 and 755 mg/kg and between 23 and 698 mg/kg in 1999 and 2008, respectively (Table 1). The highest increase of Zn reached 88%, at the northwest area of the bay (S88). In the campaign of 1999, 86% of the samples were above TEL and 25% above PEL, whereas in 2008, 80% and 36% of the samples exceeded TEL and PEL, respectively, representing an increasing risk to local biota (Table 1). Following the pattern of Cr, the highest concentrations of Zn occurred at the northwest portion of Guanabara Bay (S23, S25, S86, S88, S90, S92). Station S53, at the harbor area, also showed a high concentration of Zn, with a noteworthy increase from 1999 to 2008 (Fig. 3). The main anthropogenic sources of Zn are associated with municipal wastewater discharges, smelter slags and wastes, fertilizers, coal and bottom fly ash, wood preservatives, mine tailings, tire-wear particles and corrosion of ship hulls. Severe zinc contaminations tend to be confined to areas near the emission sources (Callender and Rice, 2000; Rice et al., 2002; Councell et al., 2004; Dong et al., 2012) therefore, results suggest a strong local contribution of this element to Guanabara Bay. Cu concentrations at Guanabara Bay had a significant increase (p¼0.025042) from 1999 to 2008 (Fig. 3), varying from 5 to 188 mg/

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kg and from 18 to 423 mg/kg, respectively (Table 1). In the first campaign, 93% of the samples presented Cu concentrations above TEL, whereas 11% were above PEL. In 2008, 100% of the samples were above TEL, and the samples that exceeded PEL, tripled (30%), characterizing potential risk for local biota (Table 1). The northwest portion of Guanabara Bay presented the highest concentrations of Cu (Fig. 2), corroborating the results found for the other trace elements evaluated in this study. Owing to the strong affinity between Cu and organic complexes (Diamond, 2012; Reuter and Perdue, 1977), it is reasonable to expect higher values of copper in the areas of the bay more enriched with organic matter. As well as for the other trace metals in this study, Cu can be introduced into Guanabara Bay through anthropogenic effluents, especially through contaminated rivers, such as Iguaçu, Sarapuí, Canal do Cunha, Mangue and Penha (Fig. 1), and also through harbor activities. Sources of Cu are usually associated with construction material, pesticides, vehicle brake pads, wood preservatives, diesel and fuel combustion, industrial facilities and marine antifouling coatings (Rice et al., 2002; Warnken et al., 2004), multiple sources that are likely to occur around Guanabara Bay. Pb concentrations (Fig. 2) also presented significant differences (p ¼0.030729) between both campaigns, with a variation from 2 to 193 mg/kg in 1999 and between 18 and 287 mg/kg in 2008 (Table 1). Samples above TEL increased from 76 to 93%, and above PEL, from 3 to 20%, between the first and second campaigns (Table 1). Similarly to the other elements evaluated in this study, the samples containing Pb concentrations above PEL, were located at the northwest portion of Guanabara bay (Fig. 2), pointing out again the strong anthropogenic input of trace elements in this area. Despite the partial or complete elimination of tetraethyl lead from gasoline since the 1990 decade in Brazil (UNEP, 1999), there are other sources of this metal that impact the environment and are usually associated with paints, pigments and batteries, and in some countries Pb is the only metal whose presence in the air is controlled by law (Vanz et al., 2003). 3.2. Background Enrichment Index The local enrichment of surface sediments of Guanabara Bay was evaluated through the New Index of Geoaccumulation (NIgeo) (Ruiz, 2001) which was determined for each metal in this study, except for Ni. In 1999 very few stations were considered nonpolluted (NIgeo o1) with respect to Cr (S28, S35, S46). On the other hand, surface sediments were already considered polluted by Zn, Cu and Pb, with values of NIgeo up to 11 for Zn, characterizing an extremely contaminated environment, and values of Igeo around 8 for Cu and Pb, indicating very polluted sediments (Table 2). With the exception of S35, all stations presented NIgeo values 47 for Zn, proving to be very contaminated sites with respect to this element, a condition favored by the elevated concentrations of organic matter and predominance of fine sediments. Zn was considered the most critical element, since 100% of the samples were Table 2 Background Enrichment Index (NIgeo) and Potential Ecological Risk Index (ERF) results for Guanabara Bay in 1999 and 2008. Indices

Cr

Zn

Cu

Pb

Ni

0.7–8.0 4.1–8.1 90 97 0–4 0–5 30 47

5.3–11.3 6.3–11.2 100 100 0–5 0–5 23 43

3.3–8.6 5.2–9.7 93 100 0–9 0–22 67 80

1.4–8.0 4.6–8.6 77 93 0–5 0–9 20 53

0.4–4.7 2.9–4.8 – – 0–1 0–2 7 10

considered very highly polluted during both sampling periods (Table 2). In the second campaign all stations were classified between moderately to extremely polluted concerning all the studied elements. The total of the samples considered very highly contaminated with Cu increased from 93 to 100% between 1999 and 2008 (Table 2). Over 90% of the stations were considered very highly polluted with Cr according to NIgeo values in 1999 and this number increased to 97% in 2008 (Table 2). Islam et al. (2015) studied an urbanized river in the northern part of Bangladesh (India) and found maximum NIgeo values of, 2.1, 1.7, 1.2 and 1.8 for Cr, Ni, Cu and Pb, respectively, whereas Wang et al. (2015) found maximum NIgeo values close to or under zero, indicating no pollution by Cu, Zn and Pb at Yangtze river (China). Both results show an enormous contrast with the ones found at Guanabara Bay, revealing its outstanding degree of contamination. 3.3. Contamination Index The Modified Degree of Contamination revealed over 56% of the samples classified as ultra-high contaminated (mCd 432) in 1999 and this number increased to 70% in 2008 (Table 3). By far, stations with higher mCd values were the ones situated at the northwest part of the bay, S86, S88, S90 and S92 (Fig. 1). Station S53, at the harbor area and close to Cunha channel and Maracanã river, two significant sources of pollution to Guanabara Bay, also showed a remarkable increase of mCd, from 75 to 132 between 1999 and 2008. Some stations that were classified as very low contaminated in 1999 (S34, S35 and S48) had a noticeable increase of mCd in 2008, becoming very high contaminated. Despite the fact that these stations present very low contents of fine sediments in their granulometric composition (Fig. 2), it is possible to suggest that the load of contaminants received in these areas is very elevated, because even low concentrations of silt and clay are able to retain high contents of trace metals. Pejman et al. (2015), used mCd to evaluate the contamination of northwest Persian Gulf and found values between 1.5 and a little higher than 2, indicating a low degree of contamination, which, compared to the results of mCd for Guanabara Bay reveals the intense degree of contamination of the study area. 3.4. Ecological Risk Indices The Ecological Risk Index (ERF) presented values higher than 1 for all the determined metals, characterizing the pollution of Guanabara Bay during both campaigns for several stations (Table 2). For Cr, 30% of the samples presented ERF41 in 1999, and this number increased to 47% in 2008. Zn presented an increase of contaminated samples from 23 to 43% between the sampling periods. Cu was the metal that presented the highest number of contaminated samples according to ERF, 67% in 1999 and 80% in 2008. The number of stations contaminated with Pb raised from 20 to 53% between 1999 and 2008. The element with the lowest level of contamination was Ni, which presented 7% of contaminated samples in 1999, with a small increase in 2008 Table 3 Mean Sediment Quality Guideline Quotient (SQG-Q), Degree of contamination (mCd) and Pollution Load Index (PLI) results for Guanabara Bay in 1999 and 2008. Indices

1999 2008 %samples with NIgeo Z5 ERF 1999 2008 %samples with ERF 41 Nigeo

Min-Max Min-Max 1999 2008 Min-Max Min-Max 1999 2008

313

SQG-Q %samples with SQG-Q Z1 mCd %samples with mDc 432 PLI %samples with PLI o 1 Total PLI for Guanabara Bay

Min-Max Min-Max Min-Max

1999

2008

0.01–1.27 7 1–81 56 0.65–2.24 37 1.12

0.23–2.14 27 9–133 70 0.47–1.72 50 0.97

314

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(Table 2). Following the pattern of previous results, the northwest portion of the study area, and the surroundings of the harbor area stood out as the most contaminated parts of this coastal bay. For Cu, however, in 2008, besides the northwest portion, the central area of the Guanabara Bay and also the northeast (S17, S30, S31, S34) were, as well, considered heavily polluted according to ERF. Indices that integrate contaminants into one value such as Sediment Quality Guideline Quotient (SQG-Q) and Pollution Load Index (PLI) allow the comparison with other ecosystems more easily. SQG-Q classified all the stations in Guanabara Bay at least as moderately impacted, and some of them were considered highly impacted (SQG-QZ1). In 1999, only 7% of the samples were considered heavily polluted, and in 2008 this number more than tripled, rising to 27% (Table 3). Most of the heavily polluted stations were located at northwest portion of Guanabara Bay, and also some at the southwest. The least polluted stations presented small concentrations of silt and clay (S35, S45, S48). S34 presented a lower concentration of silt and clay in comparison to the rest of the samples (Fig. 2), but enough to retain trace metals and be classified as polluted in both campaigns. Caeiro et al. (2005), found values of SQG-Q between 0.04 and 2.0 for the Sado Estuary in Portugal, comparable to the maximum values obtained for Guanabara Bay. The Ecological Pollution Index (PLI) by Wilson and Jeffrey (1987) resulted in small values during both campaigns for most stations (Table 3), classifying them as heavily polluted (PLI  0). In 1999 individual PLI for each station varied from 0.65 to 2.24, and in 2008, from 0.47 to 1.72. The most polluted station was S86 in both sampling periods, with a PLI of 0.65 and 0.02 in 1999 and 2008, respectively. As expected, the most contaminated sites (PLI o1) were found in the northwest and southwest portions of Guanabara Bay, during both campaigns, corroborating the results of SQG-Q. Individual PLI for each station revealed 37% of samples extremely polluted (PLI o1) (Table 3). In 2008, polluted sites (PLIo1) reached 50% of the sampled stations. The total PLI for Guanabara Bay was 1.12 in 1999 and 0.97 in 2008, showing the increase of pollution in almost a decade, classifying this coastal bay as heavily contaminated, since it approached PLI Threshold (damage to be expected¼1). The total PLI result for Guanabara Bay was comparable to very polluted systems such as Tolka, Rogerstown and Slaney estuaries in Ireland, with total PLI values of 0.78, 1.67 and 1.74, respectively; Loire and Seine estuaries in France, with total PLI values of 0.31 and 0.84, respectively, and Murrel's Inlet in the US, with a total PLI of 1.11(Wilson, 2003). Caeiro et al. (2005) found PLI station values between 0.07 and 9.60 in the Sado Estuary (Portugal), high above the maximum values obtained in this study during 1999 and 2008, 2.24 and 1.72, respectively, revealing the high level of contamination of Guanabara Bay. 3.5. Statistical analysis In general, the trace metals presented similar spatial patterns, and can be associated with the same urban and industrial sources as confirmed by the strong correlation among them showed by Principal Component Analysis (PCA) (Table 4). For the data acquired in 1999 PCA presented a total variance of 73.43%. The first axis explained 59% of the total variance in the data set, with TOC as the most significant component (Table 4), showing the influence of organic matter in the distribution of trace metals. With the exception of sand, all the components were directly and strongly correlated. The second axis explained 14.43% and the most significant component was clay, revealing the influence of fine sediments in the retention of organic matter and trace metals. For the data set obtained in 2008, PCA explained 71% of variance (Table 4), with 48.64% for the first axis and 22.36% for the second axis. The variance was dominated by the content of Zn on the first axis which reflects the fact that this was the element with the highest

Table 4 Principal Component Analysis for Guanabara Bay data in 1999 and 2008. Period Variance Ni Cr Zn Cu Pb TOC Sulfur Sand Silt Clay

1999 Factor 1 59.00% Eigenvalues
0.881
0.640
0.748
0.755
0.683
0.942
0.768 0.886
0.556
0.740

Factor 2 14.43% Eigenvalues
0.083 0.067
0.476
0.352
0.506
0.070 0.541
0.381
0.216 0.581

2008 Factor 1 48.64% Eigenvalues
0.764
0.814
0.914
0.800
0.818
0.608 – 0.546
0.341
0.451

Factor 2 22.36% Eigenvalues
0.165
0.103
0.201
0.503
0.413 0.343 –
0.817 0.461 0.716

levels of enrichment in the sediments. With the exception of sand, all the components were, again, directly correlated, suggesting similar sources for the trace metals.

4. Conclusions This study showed the markedly increase of contamination area in Guanabara Bay between 1999 and 2008, i. e., a higher number of stations exceeded the reference values for Probable Effect Level, for all the metals studied, with the exception of Ni. The northwest portion of Guanabara Bay can be considered a hot spot of trace metal contamination. The low hydrodynamic and shallow depths of this location, as well as the predominance of fine granulometric material, favor the accumulation of organic matter which serves as a trap for trace metals maintaining the high levels of contamination, as shown by multivariate statistical analysis. The metals of greatest concern were Pb and Cu, whose rise in concentrations between 1999 and 2008 were significant. Nevertheless, Zn and Cr also presented a great enrichment between sampling periods; in fact, Zn presented the highest enrichment in sediments, considering NIgeo. Aside from showing a similar spatial pattern, all elements studied seemed to have the same sources, probably the rivers and channels located in the northwest part of the bay. Results provided by the ecological indices chosen to evaluate the pollution at Guanabara Bay revealed a good accordance, since all of them pointed to the high contamination of this coastal bay. The use of Enrichment and Contamination Indices allowed comparison with other marine environments, making it possible to conclude that Guanabara Bay stands out as one of the most contaminated coastal areas in the world concerning trace metals. Despite the fact that the indices used were developed for the total fraction of trace metals, the Ecological Risk Indices suggest potential threat to local biota, what should be a matter of greatest concern considering the commercial fishing activities that take place at Guanabara Bay.

Acknowledgments FAPERJ (Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico).

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