An assessment of PCB and PBDE contamination in two tropical dolphin species from the Southeastern Brazilian coast

MPB-07255; No of Pages 7 Marine Pollution Bulletin xxx (2015) xxx–xxx

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An assessment of PCB and PBDE contamination in two tropical dolphin species from the Southeastern Brazilian coast Ricardo Lavandier a, Jennifer Arêas b, Patrick S. Dias c, Satie Taniguchi c, Rosalinda Montone c, Jailson Fulgencio de Moura d, Natalia Quinete e,⁎, Salvatore Siciliano b, Isabel Moreira a a

Departamento de Química, Pontifícia Universidade Católica do Rio de Janeiro (PUC-Rio), Rua Marquês de São Vicente, 225, Gávea - Rio de Janeiro, RJ 22453-900, Brazil Instituto Oswaldo Cruz/Fiocruz, Av. Brasil 4.365, Manguinhos, Rio de Janeiro, RJ 21040-900, Brazil Instituto Oceanográfico, Universidade de São Paulo (USP), Praça do Oceanográfico 191, Butantã, São Paulo, SP 05508-900, Brazil d Systems Ecology, Leibniz Center for Tropical Marine Ecology (ZMT), Fahrenheitstrasse 6, 28359, Bremen, Germany e Institute for Occupational and Social Medicine, Medical Faculty, RWTH Aachen University, Pauwelsstrasse 30, D-52074 Aachen, Germany b c

a r t i c l e

i n f o

Article history: Received 19 June 2015 Received in revised form 14 October 2015 Accepted 19 October 2015 Available online xxxx Keywords: PCBs PBDEs Cetaceans GC-ECNI-MS Brazil

a b s t r a c t PCBs and PBDEs were determined in two dolphin species, Sotalia guianensis and Steno bredanensis, from an upwelling system off the Central-northern coast of Rio de Janeiro, Brazil. PCB levels varied from 0.040 to 0.75 μg g−1 lw in muscles and from 0.022 to 1.32 μg g−1 lw in liver samples from S. guianensis. In S. bredanensis, values varied from 0.085 to 11.3 μg g−1 lw in muscles and from 0.024 to 18.6 μg g−1 lw in livers. PCB-138, -153 and -180 were the major PCB congeners detected in both species, while BDE-47 was the predominant PBDE congener found in both species. Higher concentrations in S. bredanensis were possibly related to the different feeding habits for both delphinid species. These results contribute to extend the database on organic contamination in cetaceans from the southern hemisphere, understanding their distribution and environmental fate in Southeastern Brazil. © 2015 Published by Elsevier Ltd.

Polychlorinated Biphenyls (PCBs) and Polybrominated Diphenylethers (PBDEs) are synthetic compounds known as persistent organic pollutants (POPs) (Magalhães et al., 2012). These contaminants are easily transported throughout the atmosphere (de Wit et al., 2006) and are able to biomagnify through the food web and bioaccumulate in fatty tissues due to their characteristic physicochemical properties, such as high hydrophobic nature and persistence in the environment (Tanabe et al., 2000). Consequently, considerable levels of these contaminants have been found in a wide range of environmental compartments and organisms (Shen et al., 2005). PCBs were widely used as dielectric fluids in capacitors and transformers (Wu et al., 2008). In Brazil, PCB production, application and commercialization were prohibited in the early 1980s (Dorneles et al., 2013). However, an interministerial decree prohibited only new equipments to work using these compounds, while old equipments containing PCBs could carry on working until replacement (Penteado and Vaz, 2001). The high stability of these compounds and their costly and technically difficult disposal forced industries to store immense amounts of PCB mixtures (Aguilar et al., 2002), resulting in a problem which still persists today. ⁎ Corresponding author. E-mail address: [email protected] (N. Quinete).

PBDEs have been used for decades as flame retardants in various products, such as furniture, electric and electronic components, insulation on wire and cable, televisions and computers (de Wit, 2002). These compounds were produced as three different formulations (Penta, Octa and Deca-BDE) (Kalantzi et al., 2009). They are structurally similar to PCBs, and show many of the same physico-chemical characteristics. The considerable levels of these contaminants found in the environment may be related to inappropriate disposal of electric and electronic products (Wong et al., 2007). Furthermore, some recent studies have demonstrated that indoor environments may be a significant source of PBDEs as they have been found in house dust and on the greasy film found on windows (Butt et al., 2004; Rudel et al., 2003). In the past decades, many populations of marine animals have declined or even became extinct, especially in coastal and estuarine areas. This may be due to habitat loss and over-exploitation (Zhou et al., 2009), however contamination by POPs may also pose health risk to marine mammals, such as cancer, immune deficiency and reproductive abnormalities (Dorneles et al., 2013), depression on the immune system (Aguilar et al., 2002) and alterations in skeletal growth and ontogenic development (Van Bressem et al., 2009). PCBs and PBDEs are known to accumulate in aquatic systems and marine mammals, such as cetaceans. Being in a higher trophic position of the food web, these animals are known to show extremely high accumulation

http://dx.doi.org/10.1016/j.marpolbul.2015.10.039 0025-326X/© 2015 Published by Elsevier Ltd.

Please cite this article as: Lavandier, R., et al., An assessment of PCB and PBDE contamination in two tropical dolphin species from the Southeastern Brazilian coast, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.10.039

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rates of these contaminants, which thus make these compounds a matter of concern regarding their toxic effects (Tanabe et al., 1994). The aim of this study was to determine PCB and PBDE levels in Guiana dolphins (Sotalia guianensis) and rough-toothed dolphins (Steno bredanensis) in order to provide baseline information on the levels, distribution and environmental fate of these contaminants in an upwelling system off the Central-northern coast of Rio de Janeiro, Brazil. Among the cetaceans found in the southern hemisphere, two species are noteworthy in Brazilian waters. The Guiana dolphin (S. guianensis) is a coastal dolphin that inhabits shallow estuaries, bays and inlets (de Moura et al., 2012), from the state of Santa Catarina, Southern Brazil, to Honduras, in Central America (Flores and Da Silva, 2009). This species feeds on pelagic and mesopelagic prey in the near-shore ecosystem (Di Beneditto and Siciliano, 2007) and exhibits high residence and site fidelity in several populations along the Brazilian coast (Santos et al., 2001). Since this is an inshore species that occupies areas closer to the potential sources of contamination due to domestic and industrial sewage (Yogui et al., 2011), this species suffers from anthropogenic impacts caused by human activities (de Moura et al., 2014). The rough-toothed dolphin (S. bredanensis) is a pelagic species widely distributed in tropical and warm temperate oceans around the world (Struntz et al., 2004). In general, this species is found in shallow nearshore, deep offshore and oceanic waters (West et al., 2011) and feeds basically on fish and mollusks (Miyasaki and Perrin, 1994). The delphinid specimens were incidentally caught in fishing nets or found stranded between the cities of Arraial do Cabo and São Francisco do Itabapoana, along the Central-northern coast of Rio de Janeiro (Fig. 1). In total, 13 specimens were recovered during regular beach patrol (8 S. guianensis individuals and 5 S. bredanensis individuals collected between 2003 and 2012). Only fresh carcasses were used in the study. Dissections were performed to obtain muscle and liver samples from each individual. Samples were then frozen at − 80 °C, freeze-dried, crushed with mortar, pestle and stored until analyses. The morphometric data and sampling site for both investigated species are displayed in Table 1. The northern region of the State of Rio de Janeiro has suffered intense urbanization in the last decades, due to the presence of major oil and gas industry centers that could be a potential source of contamination by organochlorine compounds, such as PCBs and pesticides. In this location, a local upwelling system balances the water masses. The

Table 1 Biometric data regarding S. guianensis and S. bredanensis specimens from the central-north coast of Rio de Janeiro, Brazil. Sample code

Length (cm)

Growth state

Sampling site (city)

Sotalia guianensis SG 01 M SG 02 M SG 03 M SG 04 M SG 05 F SG 06 F SG 07 F SG 08 M

Sex

182 190 183 188 201 182 186 145

Juvenile Adult Juvenile Adult Adult Adult Adult Juvenile

Quissamã Quissamã Cabo Frio Rio das Ostras São Francisco do Itabapoana São Francisco do Itabapoana São João da Barra Quissamã

Steno bredanensis SB 01 F SB 02 M SB 03 F SB 04 F SB 05 F

267 260 260 280 264

Adult Adult Adult Adult Adult

Búzios Cabo Frio Cabo Frio Cabo Frio Búzios

upwelling is most intense during the spring and summer and is due to the influence of strong and consistent East-Northeast winds. The surface water flows to the open sea and is replaced by deep waters, that are cold and nutrient-rich (Valentin et al., 1987). This phenomenon is directly linked to the trophic structure and species composition of this area (Valentin, 2001), since the increase of primary production promotes energy transfer to other trophic levels, affecting the whole food chain. This also ensures the maintenance of fish and squid stocks (De-Léo and Pires-Vanin, 2006), which, in turn, makes this area a route for many animals, including marine mammals. PBDE and PCB standards were purchased from Accustandard New Haven, CT, USA). Purities of all standards were ≥95%. All solvents used in this study were HPLC grade, and chemicals were ACS grade (J.T. Baker, Phillipsburg, NJ). PBDE reference standards (Bromodiphenyl Ether Lake Michigan Study, 10 μg mL−1 in isooctane) consisted of a mixture of 9 compounds (BDE 28, 47, 66, 85, 99, 100, 138, 153, and 154). PCB reference standards (PCB Congener Mix for West Coast Fish Studies, C-WCFS, 25 10 μg mL−1 in isooctane) consisted of a mixture of 24 PCBs: PCB 31, 33, 49, 56, 60, 70, 74, 87, 95, 97, 99, 110, 132, 141, 149, 151, 156, 158, 174, 177, 183, 194, 199, and 203. A mixture of 28 PCBs (WHO/NIST/ NOAA Congener List, C-WNN, 10 μg mL−1 in isooctane) were also used:

Fig. 1. Map of the study area.

Please cite this article as: Lavandier, R., et al., An assessment of PCB and PBDE contamination in two tropical dolphin species from the Southeastern Brazilian coast, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.10.039

R. Lavandier et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx

PCB 8, 18, 28, 44, 52, 66, 77, 81, 101, 105, 114, 118, 123, 126, 128, 138, 153, 156, 157, 167, 169, 170, 180, 187, 189, 195, 206, and 209. Approximately 1 g (dw) of homogenized sample was used and PCB103 and PCB-198 standard solutions were used as surrogates. The extraction was performed based on an Ultra-Turrax extraction, described elsewhere (de Boer et al., 2001) with minor changes as described previously (Lavandier et al., 2013; Quinete et al., 2011), consisting of three steps: Saponification, Extraction, Clean-up and Chromatographic Analysis. Briefly, in the saponification step, 20 mL of 1.0 mol L−1 of a KOH solution in absolute ethanol was added to the sample and allowed to rest for 30 min. Then the mixture was homogenized in Ultra Turrax three times: with 20 mL of acetone, 20 mL of n-hexane and 20 mL of Milli-Q water, respectively. The clean-up step was performed by an alumina column chromatography followed by treatment with sulphuric acid. The methodology used for the gravimetric determination of lipid content in biological tissues was based on the method of Bligh and Dyer (1959) with modifications proposed by Honeycutt et al. (1995). PCBs and PBDEs were analyzed by a gas chromatograph coupled to a mass spectrometer (GC–MS – Agilent Technologies 5973n) in an electron capture negative ionization mode (GC/MS-ECNI) and operated in selected ion monitoring (SIM) mode. The column HP 5MS (Agilent) used was 30 m long with a 0.25 mm internal diameter and a 0.25 mm-thick film of 5% phenyl methyl siloxane. The carrier gas was helium with a constant flow of 1.1 mL min− 1 and 1 μL of sample extract was injected at splitless mode. The temperatures for the injector, interface and ion source were 280 °C, 280 °C and 300 °C, respectively. The conditions for PCB determination were the following: the column oven was programmed for an initial temperature of 75 °C for 3 min and a rate of increase of 15 °C min−1 from 75 to 150 °C, then at a rate of 2 °C min− 1 the temperature was raised to 260 °C. Finally, the temperature was increased at a rate of 20 °C min− 1 to 300 °C and was held for 10 min. The conditions for PBDE determination were the following: the column oven was programmed for initial temperature of 70 °C for 1 min and rate of 12 °C min− 1 from 75 to 154 °C, then at a rate of 2 °C min− 1 the temperature was raised to 210 °C. Finally, the temperature increased at a rate of 3 °C min− 1 to 300 °C and held for 5 min. Blanks were analyzed in order to detect any contamination from the analytical process. They were injected after the analyses of a batch of approximately 10 samples. The calibration curves for PCBs and PBDEs were prepared in n-hexane in the following concentrations: 1, 5, 10, 20, 50, 80, 100, 150 and 200 ng mL−1, with a linear coefficient (r2) greater than or equal to 0.995. The limit of quantification (LOQ) was estimated as 10*s/S, where “s” is the standard deviation measured in blanks and “S” is the method sensitivity. For PCBs, the LOQ was between 1.36 and 4.89 ng g−1 ww (0.015 and 0.040 μg g−1 lw) and for PBDEs, between 3.40 and 4.75 ng g−1 ww (0.016 and 0.025 μg g−1 lw (Table S1). PCB-103 and PCB-198 (Accustandard) were added as standard surrogates, both at the concentration of 1.0 ng μL−1 in order to evaluate eventual losses during the analytical process and samples were spiked with a known concentration of PBDE standards at different concentrations (10 and 50 ng mL−1). Matrix spiked recoveries for PCB-103 spiked into muscle samples were in the range of 71 to 108% (Mean ± SD: 82 ± 14%) and in liver samples in the range of 67 to 104% (Mean ± SD: 83 ± 12%). For PCB 198, the recovery efficiency was in the range of 84 to 117% (Mean ± SD: 94 ± 14%) for muscles and from 87 to 115% (Mean ± SD: 92 ± 14%) in livers. The recoveries of matrix spiked with PBDEs ranged from 72 to 117% (Mean ± SD: 94 ± 15%) in muscle samples and from 68 to 121% (Mean ± SD: 91 ± 13%) in liver samples. Data normality was tested by Shapiro–Wilk W test using Statistica version 7.0. As the data showed non-normal distributions, the Kruskal–Wallis test was performed in order to determine significant differences among S. guianensis and S. bredanensis. Spearman's correlation analysis was performed, to investigate correlations between PCB and

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PBDE concentrations and dolphin morphometric variables. The level of significance was set to p b 0.05. All concentrations are expressed in lipid weight (lw). Lipid content in muscle samples varied from 4.53 to 9.32% in S. guianensis and from 2.18 to 7.44% in S. bredanensis. In liver samples, the lipid content varied between 8.48 and 20.7% in S. guianensis and 6.39 and 13.3% in S. bredanensis. The mean concentrations of PCBs in S. guianensis muscle varied from 0.040 ± 0.021 to 0.75 ± 0.34 μg g−1 lw (Mean ± SD) and from 0.023 ± 0.033 to 1.32 ± 0.97 μg g− 1 lw (Mean ± SD) in liver samples. In S. bredanensis, the mean concentrations varied from 0.085 ± 0.051 to 11.3 ± 14.3 μg g−1 lw (Mean ± SD) in muscles and from 0.024 ± 0.053 to 18.6 ± 25.4 μg g−1 lw (Mean ± SD) in liver samples. These data are presented in Table 2 for each individual. In general, PCB levels found in liver were higher than those found in muscle. Similar PCB profiles were found between muscles and liver samples for both species. Both species presented as predominant congeners PCB-138, -153 and -180, which have a long life in the environment (van der Oost et al., 2003). The major congeners found in both species were hexa-PCBs, representing approximately 35% and 42% of PCB distribution in samples of muscle and liver of S. guianensis, respectively. In S. bredanensis muscle and liver samples, hexa-PCBs represented approximately 44% and 50%, respectively, of the PCB distribution. The mean distributions of PCBs as function of their degree of chlorination are shown in Fig. 2. High percentages of hexa- and hepta-PCBs have been also found in other studies with marine mammals in Brazil and around the world (Alonso et al., 2010; Corsolini et al., 1995; Minh et al., 2000). The concentrations of these congeners may reflect the fact that these compounds were extensively used in Brazil in the form of mixtures (Lavandier et al., 2013). The mixtures containing PCB congeners marketed in Brazil were mainly imported from Germany and United States, in which the Aroclor® series was the most common (1221, 1232, 1016, 1242, 1248, 1254 and 1260) (Penteado and Vaz, 2001). Total PCB was considerably higher in S. bredanensis with concentrations up to 119. μg g−1 lipid wt in comparison to S. guianensis (9.41 μg g−1 lipid wt). A possible explanation for the differences between species may be related to their feeding habits (Ross, 2000), once S. guianensis, feed basically on small fish, squid and shrimp (Melo et al., 2010; Santos et al., 2002) while S. bredanensis feed on fish like mullet (Mugil spp.), sardine (Sardinella sp.), cutlassfish (Trichiurus lepturus) (Gurjão and Neto, Table 2 Total organic compounds (ΣPCBs and ΣPBDEs) in S. guianensis and S. bredanensis found stranded along Central-north coast of Rio de Janeiro. Sample code

Sex

ΣPCBs (μg g−1 lw) muscle

ΣPCBs (μg g−1 lw) liver

ΣPBDEs (μg g−1 lw) muscle

ΣPBDEs (μg g−1 lw) liver 0.17 0.14 0.075 0.065 0.29 0.23 0.066 0.14 0.15 0.076

Sotalia guianensis SG 01 M SG 02 M SG 03 M SG 04 M SG 05 F SG 06 F SG 07 F SG 08 M Mean SD

8.74 4.65 4.97 3.88 12.5 7.01 3.26 5.68 6.34 2.86

9.99 5.37 9.39 5.64 26.3 11.4 1.52 5.72 9.41 7.02

0082 0.072 0.046 0.052 0.14 0.10 0.030 0.069 0.074 0.033

Steno bredanensis SB 01 F SB 02 M SB 03 F SB 04 F SB 05 F Mean SD

19.5 174.7 152.6 5.55 3.63 71.2 76.0

17.6 192.2 353.2 7.83 28.0 119.8 134.9

0.051 0.71 0.63 0.13 0.031 0.31 0.30

0.15 1.10 1.29 0.31 0.13 0.60 0.50

Please cite this article as: Lavandier, R., et al., An assessment of PCB and PBDE contamination in two tropical dolphin species from the Southeastern Brazilian coast, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.10.039

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R. Lavandier et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx

Fig. 2. Mean residual patterns of PCB congeners in both dolphin species.

2004). Larger prey and top-predator fish accumulate larger amount of contaminants in their bodies, thus rough-toothed dolphins are more likely to uptake higher amounts of organic contaminants. This difference between S. guianensis and S. bredanensis was also observed by Dorneles et al. (2013). Another important factor could be the age difference between the sampled individuals from the two analyzed species (Yogui et al., 2003). There are still few reports on these contaminants in muscle samples of both studied species, with most studies conducted in blubber and liver samples. However, PCB levels found in the present study were in the same order of magnitude as the study conducted by Quinete et al. (2011). For S. guianensis, the mean concentrations found in this study are in the same order of magnitude as other studies regarding this species' blubber, such as the study conducted by Santos-Neto et al. (2014) in the Northeastern coast of Brazil, by Yogui et al. (2003) in individuals found stranded in Cananéia estuary in the state of São Paulo, Southeastern coast of Brazil, and in liver samples by Lailson-Brito et al. (2010) in three different estuaries of the Brazilian Southern and Southeastern coasts. Guiana dolphins in the present study showed concentrations an order of magnitude lower when compared to other studies regarding this species, such as the study conducted by Dorneles et al. (2013) at Guanabara Bay, in the state of Rio de Janeiro, which is the area mostly impacted by anthropogenic activities along the Brazilian coast. The levels in the present study were also lower than those found in the studies of Kajiwara et al. (2004). Mean PCB concentrations in the present study are lower than those reported in different cetaceans from industrialized areas around the world, such as the levels reported in two estuaries in the United States Coast by Fair et al. (2010), in the Mediterranean Sea (Corsolini et al., 1995) and in the Japanese Coast (JEA, 1999). The concentrations in liver of S. bredanensis found in this study were about an order of magnitude higher than those levels reported in other studies regarding this species' blubber, such as in the study of Yogui et al. (Yogui et al., 2010) in São Paulo. Besides that, our levels are also higher than those found in industrialized areas around the world, such as in the study by Marsili and Focardi (1997) along the Italian coast, and by Struntz et al. (2004) in Florida, USA. Similar results were found in S. bredanensis blubber by Lailson-Brito et al. (2012). A possible reason for the higher PCB concentrations observed in the present study for S. bredanensis could be related to the coastal distribution of this species, their feeding habits and also the age of the dolphins, which were all adults. The levels observed here are of great concern since they seem to suggest the presence of PCB contamination sources in the CentralNorthern region of Rio de Janeiro Coast, which may be related to the close proximity to the major urban centers of the oil and gas industry of Brazil, located in the cities of Campos dos Goytacazes and Macaé (Totti and Pedrosa, 2006). Another factor is the proximity of these cities to the Paraíba do Sul River, which originates in the State of São Paulo and flows in the Atlantic Ocean at the city of São João da Barra. The river is 1145 km long and is

the largest river in southeastern Brazil, flowing through the most important industrial regions of the country (Rio de Janeiro and São Paulo). This river is heavily contaminated by agricultural runoff and discharges from untreated industrial and domestic wastes (Linde-Arias et al., 2008; Quinete et al., 2011). The mean concentrations of PBDEs in muscle of S. bredanensis ranged from 0.013 ± 0.011 to 0.043 ± 0.018 μg g−1 lw (Mean ± SD) and in liver from 0.026 ± 0.016 to 0.084 ± 0.048 μg g−1 lw (Mean ± SD). In S. bredanensis, the mean concentration in muscles varied from 0.043 ± 0.046 to 0.19 ± 0.21 μg g−1 lw (Mean ± SD) while in liver samples from 0.11 ± 0.079 to 0.35 ± 0.36 μg g−1 lw (Mean ± SD). Only three congeners were above the limit of quantification in all samples of S. guianensis and S. bredanensis (BDE-47, -99 and -100) and the distribution of the congeners decreased in the following order BDE-47 N BDE100 N BDE-99. The concentrations of PBDEs were also higher in S. bredanensis than in S. guianensis and these differences may be attributed to the same previous reasons discussed before for PCBs. The ΣPBDEs ranged from 0.029 to 0.28 μg g−1 lw in muscle and liver of S. guianensis while for S. bredanensis, ΣPBDEs ranged from 0.031 to 1.30 μg g−1 lw, showing to be higher in liver than in muscle samples. The concentrations are presented in Table 2 for each individual and the mean distribution for PBDEs in samples of S. guianensis and S. bredanensis are presented in Fig. 3. The predominant congener in this study was BDE-47 and according to Quinete et al. (2011), the presence of BDE-47, -99 and -100 suggests the possible use of a commercial Penta-BDE mixture in Brazil. A similar profile was reported in marine mammals from North America (Ikonomou and Addison, 2008) and in white crappie fish (Dodder et al., 2002), where Penta-BDE has been extensively used. Penta- and Octa-BDE were banned from the market in Europe and United States in the last decade, since these compounds were classified as POPs by the Stockholm Convention (Alonso et al., 2014). However, the ban of Deca-BDE formulation in electrical and electronic equipment throughout Europe occurred years later, in 2008 (European Court of Justice, 2008) and in some U.S. states, the ban occurred only in 2013 (Alonso et al., 2014). In Brazil, PBDE-containing products in the country (either imported or produced in Brazil) must have concentrations lower than 0.1%, but this restriction includes only computers, computer accessories and components (Brasil, 2009). The presence of these congeners, even in low levels, is of great concern due to the fact that PBDEs are emerging pollutants, which may be carcinogenic, cause neurotoxic effects and also act as endocrine disrupters (Darnerud, 2003; Richardson et al., 2008). Even though PCBs, DDTs and PBDEs have showed a decreasing trend in mammals and environmental levels since their ban and restrictive regulation regarding their production and use, PCB levels have stabilized over the years and levels found in marine mammals are often far above the accepted toxicological threshold values (Law, 2014; Law et al., 2012). In fact, PCB levels found in both species exceeded in most samples the threshold

Please cite this article as: Lavandier, R., et al., An assessment of PCB and PBDE contamination in two tropical dolphin species from the Southeastern Brazilian coast, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.10.039

R. Lavandier et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx

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Fig. 3. Mean residual patterns of PBDE congeners in both dolphin species.

concentrations (6.60–11.0 μg g−1 lw of total PCBs) for PCBs in liver of aquatic mammals known to cause adverse effects on immune function (Kannan et al., 2000). The PBDE levels found in the present study for S. guianensis were an order of magnitude lower than those found by Dorneles et al. (2010), which reflects the pollution of Guanabara Bay, the most impacted area in Brazil, and Quinete et al. (2011) in S. guianensis found stranded close to the mouth of Paraíba do Sul River. However, PBDE concentrations in our study were similar to those presented in the study of Yogui et al. (2011), regarding this species from the Brazilian Southeastern coast. Our data were also similar to previous reports in fish from some locations of the United States, China and Chile (Montory et al., 2010; Shen et al., 2009; Staskal et al., 2008). S. bredanensis samples presented similar concentrations to previous studies for this species in Brazil, United States and Italy (Pettersson et al., 2004) (Dorneles et al., 2010; Tuerk et al., 2005). Both species in the present study presented lower levels when compared to blubber samples from other studies in industrialized regions of the world, such as in the United States (Fair et al., 2010; Kuehl and Haebler, 1995), United Kingdom (Law et al., 2005) and in Asian waters (Kajiwara et al., 2006). Even though levels in the Southern hemisphere are lower than those in the Northern hemisphere, PCB contamination is of great concern, especially since these concentrations have stalled over the years at toxicologically significant levels and could then constitute potential health and environmental risk to these ecosystems. The concentrations of all contaminants varied significantly when comparing intra-species data. Generally, older males have the highest levels of POPs in cetaceans (Addison, 1989), since females may transfer POPs during pregnancy and via milk during lactation (Wells et al., 2005). Interestingly, in the present study, generally, the female individuals from both species presented the highest PCB and PBDE levels. Although some males showed also high PCB and PBDE levels. The contamination pattern in aquatic mammals can be related to age, since age-dependent accumulation of POPs is more common in higher animals (Subramanian et al., 1988). In fact, high concentrations of these contaminants were found in an individual whose body length was of 201 cm, which was probably an adult according to Siciliano et al. (2007). According to Ramos et al. (2000), the Guiana dolphins from northern Rio de Janeiro reach sexual maturity at six years for both genres and at 180 cm of body length for males and 160 cm for females. In this study, a juvenile showed similar concentrations of PCBs and PBDEs to adult individuals, suggesting mother transfer during pregnancy and via milk during lactation (Wells et al., 2005). Among the S. bredanensis specimens, two adult female individuals collected in this study showed the lowest concentrations of the studied compounds. In the case of individual SB 04, milk was found in its breast,

which corroborates the hypothesis of mother transfer during pregnancy (Borrell, 1993) and lactation (Tanabe et al., 1994). It has been estimated that in cetaceans about 60–100% of organic contaminants in the body of the mother are transferred to the newborn through lactation due to the high lipid content in the milk of these animals and the physicochemical properties of POPs, although during pregnancy around 10% of total body burdens could be transferred also through the placenta (Borrell et al., 1995; Stringer and Johnston, 2001). Regarding PCB and PBDE concentrations, no significant differences were observed when muscle and liver samples were compared for each species separately, although concentrations were higher in livers. However, when comparing PCB levels in muscle samples of S. guianensis and S. bredanensis, a significant difference was observed (p value = 0.002054) and the same for liver samples of both species (p value = 0.001803). A significant positive correlation was observed between tri-PCBs and sex in S. guianensis muscle samples (r = 0.85). Significant positive correlations were observed between hepta-PCBs and lipid content in S. guianensis muscle samples (r = 0.72). In this species liver samples, tri-, tetra-, penta-, hexa-, hepta- and octa-PCBs showed strong positive correlations with lipid content (r, respectively, = 0.95; 0.96; 0.94; 0.80; 0.75; 0.80). In S. bredanensis, positive correlations were also found between lipid content and octa- and nona-PCBs (r, respectively = 0.90; 0.90). This is expected, since lipophilicity increases with the increasing of the degree of chlorination, confirming the lipophilic properties of these compounds (Iwata et al., 1994; Mazet et al., 2005). Finally, a positive correlation between BDE-47 and lipid content was also observed in liver samples of S. guianensis (r = 0.73). No correlations were found between PBDE concentrations and lipid content for both muscle and liver of S. bredanensis. In some other studies, correlations were also found between lipid content and the total concentration of organic pollutants (Leonel et al., 2012; Marsili and Focardi, 1997; Quinete et al., 2011; Yogui et al., 2011). In summary, considerable high PCB and PBDE levels were observed in muscle and liver samples of S. guianensis and S. bredanensis from the Central-northern coast of Rio de Janeiro, Southeastern Brazil, suggesting the existence of a PCB contamination source in Brazil. Concentrations were generally higher in liver than muscle, although no statistical difference was observed for both species. Higher chlorinated PCB-138, -153 and -180 were the major PCB congeners detected in both species, while BDE-47 was the predominant PBDE congener found in both species. The analyzed POPs were significantly higher in S. bredanensis when compared to S. guinanesis, possibly related to their different feeding habits. This baseline information complements the database on organic contamination in cetaceans from Brazil, leading to a more complete understanding on the distribution and environmental fate of these pollutants.

Please cite this article as: Lavandier, R., et al., An assessment of PCB and PBDE contamination in two tropical dolphin species from the Southeastern Brazilian coast, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.10.039

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Please cite this article as: Lavandier, R., et al., An assessment of PCB and PBDE contamination in two tropical dolphin species from the Southeastern Brazilian coast, Marine Pollution Bulletin (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.10.039