Persistent organic pollutants in ringed seals from the Russian Arctic

Science of the Total Environment 409 (2011) 2734–2745

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Persistent organic pollutants in ringed seals from the Russian Arctic Vladimir Savinov a, Derek C.G. Muir b, Vladislav Svetochev c, Olga Svetocheva c, Stanislav Belikov d, Andrey Boltunov d, Ludmila Alekseeva e, Lars-Otto Reiersen f, Tatiana Savinova a,g,⁎ a

Akvaplan-niva, Polar Environmental Centre, N-9296, Tromsø, Norway Aquatic Ecosystem Protection Research Division, Environment Canada, Burlington, Canada Murmansk Marine Biological Institute, Russian Academy of Sciences, 183010, Murmansk, Russia d All-Russia Research Institute on Nature Protection, Sadky-Znamenskoe, Moscow, Russia e Centre for Environmental Chemistry, SPA “Typhoon”, Obninsk, Russia f AMAP Secretariat, Oslo, Norway g University of Tromsø, N-9037, Tromsø, Norway b c

a r t i c l e

i n f o

Article history: Received 17 August 2010 Received in revised form 22 February 2011 Accepted 23 February 2011 Keywords: Russian Arctic Ringed seals PCBs PCDD/Fs PBDEs OCs

a b s t r a c t Organochlorine compounds total DDT (ΣDDT), total HCH isomers (ΣHCH), toxaphenes (sum of Parlar 26, 50, 62), mirex, endrin, methoxychlor, total chlorinated benzenes (ΣCBz), total chlordane compounds (ΣCHL), polychlorinated biphenyls (total of 56 congeners; ΣPCBs), polychlorinated dibenzo-p-dioxins and furans (PCDD/Fs), and polybrominated diphenyl ethers (sum of 7 tri- to hepta congeners; ΣPBDEs) were analysed in the blubber of adult ringed seals from the four areas of the Russian Arctic (White Sea, Barents Sea, Kara Sea and Chukchi Sea) collected in 2001–2005. Ringed seals from the south-western part of the Kara Sea (Dikson Island — Yenisei estuary) were the most contaminated with ΣDDTs, ΣPCBs, ΣCHL, and mirex as compared with those found in the other three areas of Russian Arctic, while the highest mean concentrations of ΣHCHs and PCDD/Fs were found in the blubber of ringed seals from the Chukchi Sea and the White Sea, respectively. Among all organochlorine compounds measured in ringed seals from the European part of the Russian Arctic, concentrations of ΣDDT and ΣPCBs only were higher as compared with the other Arctic regions. Levels of all other organochlorine compounds were similar or lower than in seals from Svalbard, Alaska, the Canadian Arctic and Greenland. ΣPBDEs were found in all ringed seal samples analysed. There were no significant differences between ΣPBDE concentrations found in the blubber of ringed seals from the three studied areas of the European part of the Russian Arctic, while PBDE contamination level in ringed seals from the Chukchi Sea was 30–50 times lower. ΣPBDE levels in the blubber of seals from the European part of the Russian Arctic are slightly higher than in ringed seals from the Canadian Arctic, Alaska, and western Greenland but lower compared to ringed seals from Svalbard and eastern Greenland. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Bioaccumulation and widespread distribution of persistent organic pollutants (POPs) have been reported for ringed seals (Phoca hispida) from different Arctic regions and summarised in the AMAP POPs assessment reports (de March et al., 1998; de Wit et al., 2004, 2010; AMAP, 2009). However, relatively few data exist from the Russian Arctic, which have shown to have high concentrations of many organochlorine compounds (OCs), especially PCBs and toxaphene in tissues of ringed seals from the Barents, Kara and White Seas (Nakata et al., 1998; Wolkers et al., 1998; Kostamo et al., 2000; Savinova et al., 2000; Muir et al., 2003). At a time when human activity in the Russian

⁎ Corresponding author at: Akvaplan-niva, Polar Environmental Centre, N-9296, Tromsø, Norway. Tel.: + 47 77644901. E-mail address: [email protected] (T. Savinova). 0048-9697/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2011.02.039

Arctic (shipping, oil and gas development etc.) is increasing exponentially, contaminant loads in marine ecosystems may have negative impact on marine animals and indigenous human populations. Ringed seals are the most numerous and widely distributed high Arctic pinniped species. They are the main prey species of polar bears and the most important natural resource for many indigenous people in coastal areas of the circumpolar Arctic. The world population of ringed seal is at least a few million (Stirling and Calvert, 1979; Reeves, 1998). Ringed seal is a widespread seal species in seas of Russian Arctic including the White, Barents, Kara and Chukchi Seas. The last observations (Gepner, 1976; Svetochev and Svetocheva, 1995) indicate a stable White Sea ringed seal population (20–24,000 animals). Number of seals in the Barents Sea estimated is approximately 50,000 animals, of which about 20,000 are in the southeastern part of the sea (Pechora Sea area) (Chapsky, 1940; Ognetov et al., 2003). The Kara Sea ringed seal population is about 150,000

V. Savinov et al. / Science of the Total Environment 409 (2011) 2734–2745

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Fig. 1. Map of the Russian Arctic and ringed seal sampling sites, 2001–2005.

animals, among them 15,000 are in the south-western part of the sea and about 40,000 in the Yenisei region (Chapsky, 1940; Ognetov et al., 2003). The estimated abundance of ringed seals in the eastern Chukchi Sea is about 200–250,000 animals (Bengtson et al., 2005). The primary route of marine mammal exposure to POPs is consumption of contaminated prey. Fish (arctic cod, sculpins, whitefishes and salmon,) and crustaceans (amphipods, shrimp and Mysidacea) are major prey of ringed seals in the White, Barents and Kara seas (Svetocheva, 2002). In Chukchi Sea, the important food species for ringed seals are arctic cod, saffron cod, shrimps, and other crustaceans. To increase information on baseline levels of POPs in ringed seals from the Arctic, contemporary concentrations of a wide range of POPs were determined in the blubber of ringed seals collected from four regions of the Russian Arctic. The levels and patterns of POPs were compared among seals from the four sampling regions as well as to those reported previously in ringed seals from other regions of the Arctic (e.g., Greenland, Alaska). Differences in concentrations of POPs between male and female seals were also examined. 2. Material and methods 2.1. Sample collection, storage and handling Adult ringed seals were caught in the White Sea (Kalgalaksha Bay) (September–October 2001), south-eastern Barents Sea (Vaygach Island) (February–March 2002), south-eastern Kara Sea (Dikson Island — Yenisei estuary) (May 2002) and south-western coast of the Chukchi Sea (Vankarem) (November 2005) (Fig. 1) with permission from the Russian environmental authorities. Body mass (of the White Sea ringed seals only) and body length were measured,

and sex was recorded (Table 1). Blubber (20 g) for POP analyses was sampled from the ventral mid-line between the front flippers. A tooth was extracted for age determination. Blubber samples were wrapped in aluminium foil and placed into a thermos bottle with freezer elements for 2–4 h before they were stored in a freezer at − 20 °C. Age determination was performed by examination of the annual growth layer groups in dentine zones in tooth sections (Klevezal, 1988). 2.2. Chemical analyses and quality assurance The following persistent organic pollutants (POPs) were determined at the Centre of Environmental Chemistry, S.P.A. Typhoon (Obninsk, Russia): DDT-family (o,p′-DDE, p,p′-DDE, o,p′-DDD, p,p′DDD, o,p′-DDT, and p,p′-DDT); chlorinated benzenes (CBz) (tri-, tetra-, penta- and hexachlorobenzene); hexachlorocyclohexanes (HCHs) (α-, β- and γ-isomers); chlordane compounds (oxychlordane, cis- and trans-chlordane, trans-nonachlor, heptachlor); mirex, endrin, methoxychlor; toxaphene congeners (Parlar 26, 50, 62), polychlorinated biphenyls (PCBs), including non-ortho and mono-ortho — substituted congeners: PCB-77, 81, 105, 114, 118, 123, 126, 156, 157, 167, 169, and 189; polybrominated diphenyl ethers (PBDEs): BDE-28, 47, 99, 100, 153, 154 and 183, and polychlorinated dibenzo-p-dioxins and furans (PCDD/Fs): 2,3,7,8-TeCDD, 1,2,3,7,8-PeCDD, 1,2,3,4,7,8-HxCDD, 1,2,3,6,7,8-HxCDD, 1,2,3,7,8,9-HxCDD, 1,2,3,4,6,7,8-HpCDD, OCDD, 2,3,7,8-TeCDF, 1,2,3,7,8-PeCDF, 2,3,4,7,8-PeCDF, 1,2,3,4,7,8-HxCDF, 1,2,3,6,7,8-HxCDF, 2,3,4,6,7,8-HxCDF, 1,2,3,7,8,9-HxCDF, 1,2,3,4,6,7,8HpCDF, 1,2,3,4,7,8,9-HpCDF and OCDF. A 5 g aliquot of the homogenate was transferred quantitatively to large mortars and 150 g of anhydrous Na2SO4 was added. The sample mixture was ground manually until a free-flowing mixture resulted. This mixture was transferred into a 300 mm× 45 mm o.d. chromatography

Table 1 Biological parameters of ringed seals (Phoca hispida) collected in 2001–2005. Region

White Sea White Sea Barents Sea Barents Sea Kara Sea Kara Sea Chukotka Chukotka N.d. = no data.

Sampling area

Kalgalaksha Bay Kalgalaksha Bay Vaygach Island Vaygach Island Dikson Island Dikson Island Vankarem Vankarem

Sex

Female Male Female Male Female Male Female Male

Number

9 15 2 6 3 3 2 2

Age, year

Weight, kg

Length, cm

Mean ± S.D.

Mean ± S.D.

Mean ± S.D.

6.4 ± 2.9 6.5 ± 3.1 4.0 ± 1.4 4.3 ± 2.2 15.3 ± 11.9 13.3 ± 12.7 N.d. N.d.

51.4 ± 8.2 47.5 ± 8.9 N.d. N.d. N.d. N.d. N.d. N.d.

111 ± 8.1 108 ± 10.1 94.5 ± 6.4 105 ± 14.6 111 ± 15.9 113 ± 2.5 N.d. N.d.

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column and was spiked directly on the homogenate with surrogate mixture containing OCN (octa-chlornaphtalene) and delta-HCH (nonlabelled isomer of HCH) to control recovery of OCs, and PCB 30, PCB 204 to control recovery of PCBs. The column bed was eluted with 300 ml of hexane:dichloromethane (1:1 by volume). Samples were concentrated by rotary evaporation and percent extractable lipid content was determined gravimetrically before concentrated H2SO4 was used to remove lipids. Fractionation was accomplished with 3 g of 3% deactivated silica gel column eluted with 20 ml of hexane (fraction 1, containing PCBs, HCB and DDE) and 20 ml of hexane:DCM (1:1) (fraction 2, containing OCs). All fractions were concentrated by a combination of rotary evaporation and nitrogen evaporation and performance standard (PCB 166) was added before analysis. Each fraction was injected into a gas chromatograph (Hewlett Packard 5790A) equipped with 63Ni electron capture detector and a 25 m long 0.25 um HP-1 capillary column. This method of analysis was developed under contract for Environment Canada and a detailed method description and GC conditions are given in Muir et al. (2003). Toxaphenes, PCDD/PCDF(congeners), and PBDEs were determined by GC/LRMS (low resolution) Varian CP3800/Saturn 1200 using chemical ionisation mode with detection of negative ions (NCI) in the selective ion monitoring. Calibration of the instrument was carried out using standard solutions of Toxaphenes (TOX 482, Promochem), standard solutions of PCDD/PCDF prepared on the basis of the mixture EDF 7999 (Cambridge Isotope Lab.) and standard solutions of PBDE prepared using the mixture EO-4980 (Cambridge Isotope Lab). Results of analyses were processed with software package Varian 5.2. PCBs and pesticides were quantified using certified external standard solutions obtained from the National Laboratory for Environmental Testing in Burlington, Canada. A detailed description of extraction and analyses is given in Muir et al. (2003). Laboratory routinely analysed duplicate samples and blank samples in parallel with samples as well as certified reference materials. The quality assurance (QA) included: analysis of a National Institute of Standards and Technology (NIST) cod liver oil reference material (SRM 1588), reagent blanks, duplicates every 5 samples and internal standards of δ-HCH, CB30, CB204 and OCN in all samples. Blank samples consisting of all laboratory reagents were analysed every 10 samples. Low levels of chlorobenzenes, DDT-related compounds and PCB congeners were found in blanks, however, they were consistently less than 2% of the observed levels in seal blubber, therefore, no blank correction was performed for seal blubber. Concentration of PBDE congeners in procedural blanks (ranging from 4.3 to 28 pg) were taken into account in the calculation of contents of PBDEs in samples. No polychlorinated dibenzo-p-dioxins and dibenzofurans were found in any procedural blanks (bMDL). Method detection limit (MDL) was defined as 3 times the standard deviation (S.D.) of blank measurements or as lowest calibration standard if blank was zero. Recoveries of internal standards δ-HCH, CB 204, CB30 and OCN averaged 91%, 94%, 80% and 72%, respectively. Results for duplicates varied by less than 30% for all major OC analytes. The cod liver standard reference material from National Institute of Standards and Technology (Gaithersburg MD) was analysed in triplicate prior to the start of the seal blubber analyses. Values for almost all analytes were within 30% of the certified value, except for heptachlor epoxide and endrin which were partially destroyed by the concentrated H2SO4 step. During sample analyses the laboratory successfully participated in the Quality Assurance Laboratory Performance Studies for Environmental Measurements in Marine Samples (QUASIMEME) laboratory performance exercises on POPs in biota and sediment and in the AMAP Ring test on the toxaphene determination in serum in 2003 and in the intercalibration study on PCDD/F; PCBs, PBDE determination in fish, soil and ash with the University of Umeå (Sweden).

2.3. Statistical data treatment Concentrations were log transformed to yield normally distributed data (Shapiro–Wilk's W Test). T-tests were used with the logtransformed data for pairwise comparison of the geometric mean contaminant concentrations in each area. Null hypotheses (equality of means) were rejected at the 95% significance level (p b 0.05). The word “significant” has been used only in the statistical context and is taken to mean that statistical testing indicated a probability of chance occurrence of less than 5%. All statistical procedures were performed using STATISTICA version 5.5, StatSoft, Inc. 3. Results and discussion 3.1. Concentrations and geographical differences 3.1.1. Major persistent organic pollutants The results for measurements of POPs in the blubber of ringed seals from the selected areas of Russian Arctic are presented in Table 2. Data on PCBs (coplanar PCBs excluded), DDT, chlordanes, dieldrin, mirex, chlorobenzenes and HCH in the blubber of ringed seals from the White Sea have been published previously (Muir et al., 2003). Concentrations of major organochlorines in the blubber of ringed seals from the studied areas decreased in orders: ΣPCB N ΣDDT N ΣCBz N ΣCHL N ΣHCH (Kalgalaksha Bay); ΣPCB N ΣDDT N ΣCHL N ΣCBz N ΣHCH (Vaygach Island); ΣDDT N ΣPCB N ΣCHL N ΣHCH N ΣCBz (Dikson Island), and ΣPCB N ΣHCH N ΣDDT N ΣCHL N ΣCBz (Vankarem). 3.1.2. DDT The technical dichlorodiphenyltrichloroethane (DDT) consists of parent DDT compounds (p,p′-DDT and its o,p′-substituted isomer) as well as their dechlorinated analogues (p,p′- and o,p′-DDD). In the former Soviet Union, the mass production of DDT began in 1946 (Fedorov, 1999) where it was the one of the most widely used and produced pesticides. Although DDT was officially banned in 1970, its usage continued until early 1990s. The total DDT usage in the former Soviet Union during the 1946–1990 period has been estimated in the range from 250,000 tonnes to 520,000 tonnes (Li et al., 2006). Elevated levels of DDT were also detected in Russian rivers Ob and Yenisei (Melnikov et al., 2002; Carroll et al., 2008), indicating recent introduction of DDT into the Ob drainage basin. ΣDDT (sum of o,p′-DDE, p,p′-DDE, o,p′-DDD, p,p′-DDD, o,p′-DDT and p,p′-DDT) concentrations ranged as 293–1360 ng/g lw, 303– 1920 ng/g lw, 570–7130 ng/g lw, and 21–119 ng/g lw in the blubber of seals from Kalgalaksha Bay, Vaygach Island, Dikson Island, and Vankarem, respectively. There were no significant differences between ΣDDT concentrations found in the blubber of male and female individuals from Kalgalaksha Bay, Vaygach Island and Vankarem. However, geometric mean ΣDDT concentration measured in the blubber of male seals from Dikson Island (3650 ng/g lw) was significantly higher than found in the blubber of female (858 ng/g lw) from the same site. These values are quite similar (for male) or lower (for female) to those found in the blubber of ringed seals collected in the same area in 1995 (Nakata et al., 1998) (3600 and 2300 ng/g lw, respectively). The DDT-family compounds were the only contaminants studied that has showed significant inter-sexual differences in concentration. Therefore mean values used in the subsequent discussion have been calculated for both sexual groups integrally. There was no statistically significant difference between geometric mean concentrations of ΣDDT found in seals from Kalgalaksha Bay (530 ng/g lw) and Vaygach Island (619 ng/g lw), however, these values were significantly lower as compared with Dikson Island (1770 ng/g lw) and significantly higher than in ringed seals from Vankarem (54 ng/g lw). The highest ΣDDT level found in the blubber of ringed seals from Dikson Island is probably a consequence of DDT

Table 2 Concentrations of chlorinated pesticides (ng/g lw), chlorobenzenes (ng/g lw), polychlorinated biphenyls (PCBs) (ng/g lw), toxaphenes (Parlars) (ng/g lw), polybrominated diphenyl ethers (PBDE) (ng/g lw); polychlorinated dibenzo-pdioxins (PBDDs) and furans (PBDFs) (pg/g lw), toxic equivalents(TEQs) (pgTEQ/g lw) and content of lipids (%) in blubber of ringed seal from the Russian Arctic. Range and geometric means (GMs). POPs

Vaygach Island, Barents Sea

Dikson Island, Kara Sea — Yenisei estuary

Female, N = 9

Female, N = 2

Female, N = 3

Male, N = 15

Male, N = 6

Vankarem, Chukotka Peninsula

Male, N = 3

Female, N = 2

Male, N = 2

Range

GM

Range

GM

Range

GM

Range

GM

Range

GM

Range

GM

Range

GM

Range

7.47–23.8 b0.02–13.0 0.73–6.66 11.1–32.8 9.79–94.5 b0.02–2.16 b0.02–0.98 b0.02 b0.05–0.20 10.1–95.5 b0.02–0.52 b0.02–3.09 b0.05–3.90 298–488 b0.05–1.81 3.63–18.9 0.54–10.8 80.1–245 392–736 b0.05–1.05 b0.05–4.17 b0.05 1.02–5.53 2.23–27.0 b0.02–27.6 0.38–5.02 b0.02–7.62 10.0–17.6 25.8–61.0 497–1150 136–420 727–1850 1.78–73.2 2.11–62.7

12.7 0.26 2.34 18.0 32.9 0.04 0.04 b 0.02 0.04 33.5 0.02 0.02 0.18 350 0.22 11.2 3.69 134 505 0.08 0.22 b 0.05 2.97 8.31 4.47 1.84 1.40 13.5 43.1 734 223 1120 4.64 5.41

4.91–18.5 b0.02–22.5 0.19–9.95 8.51–43.1 6.00–86.4 b0.02–2.73 b0.02–0.62 b0.02 b0.05–1.74 6.50–87.1 b0.02 b0.02 b0.05–4.52 220–1130 b0.05–8.64 5.66–27.0 b0.05–9.91 57.3–270 293–1360 b0.05–12.1 b0.05–8.36 b0.05 1.00–12.3 2.11–22.7 b0.02–19.3 0.24–7.04 b0.02–6.58 8.88–19.1 27.6–52.0 374–1620 152–387 579–2420 1.28–16.2 2.92–15.0

11.7 0.24 2.52 19.1 30.7 0.05 0.02 b 0.02 0.05 31.5 b 0.02 b 0.02 0.17 381 0.68 12.1 3.58 139 546 0.21 0.19 b 0.05 2.87 8.96 4.01 2.08 0.79 12.4 38.9 667 223 1060 4.22 5.51

7.79;16.7 4.39;6.19 0.90;1.91 13.1;24.8 41.0;209 1.15;1.96 1.87;3.26 0.70;1.67 b 0.05 44.7;216 b 0.02 b 0.02 6.54;16.6 494;1760 b 0.05 4.43;25.7 2.55;8.54 23.2;104 531;1920 0.70;3.53 b 0.05 b 0.05;3.76 b 0.02;0.31 23.4;24.8 b 0.02;0.07 1.29;3.07 3.09;3.35 11.5;17.4 39.5;48.8 449;1040 115;347 630;1490 0.80;1.63 2.07;3.50

11.4 5.21 1.31 18.0 92.5 1.50 2.47 1.08 b0.05 98.2 b0.02 b0.02 10.4 933 b0.05 10.7 4.67 49.1 1010 1.57 b0.05 0.34 0.06 24.1 0.03 1.99 3.22 14.1 43.9 684 200 970 1.14 2.69

3.80–16.2 2.03–11.4 0.68–2.27 6.52–24.1 47.5–131 0.69–1.53 1.33–2.56 0.20–1.78 b0.05 50.8–136 b0.02–0.47 b0.02–1.76 5.38–13.8 210–820 b0.05–0.32 3.05–14.3 3.68–10.7 17.6–101 303–860 1.40–2.92 b0.05 b0.05–6.29 b0.02–0.49 0.01–35.1 b0.02–0.37 1.63–2.76 1.17–7.37 7.64–20.5 11.7–59.5 380–729 83.0–197 614–1110 0.69–3.67 1.54–4.93

9.70 3.95 1.29 15.4 82.8 1.05 1.79 0.79 b0.05 86.7 0.04 0.05 7.08 444 0.09 6.77 5.78 47.1 526 2.21 b0.05 1.30 0.11 1.08 0.05 2.00 3.44 12.3 29.3 538 136 798 1.61 2.80

13.2–43.4 6.35–20.2 1.87–2.95 21.5–65.5 85.6–195 1.45–3.08 0.73–5.59 1.60–5.40 b0.05 90.4–208 b0.02–0.56 b0.02–7.17 5.38–35.4 490–1020 b0.05–3.60 23.3–53.4 8.32–22.6 35.2–130 570–1200 4.27–12.6 b0.05 1.70–6.04 b0.02–0.62 b0.02–29.2 b0.02–0.29 b0.02–2.33 5.42–9.24 6.45–11.6 20.6–51.8 442–767 235–412 644–1310 3.57–12.91 2.40–9.42

22.9 11.5 2.18 36.9 119 2.09 1.95 3.49 b0.05 127 0.13 0.75 12.9 708 0.54 31.4 15.0 76.7 858 6.31 b0.05 2.73 0.14 1.94 0.03 0.34 6.93 9.30 34.2 631 295 981 6.70 4.90

13.8–19.6 9.25–14.7 0.44–5.64 26.0–39.9 158–843 3.90–12.7 1.30–2.41 1.80–38.56 b0.05 173–896 b0.02–1.47 b0.02–11.1 13.5–52.6 1430–6190 b0.05–1.81 22.5–168 7.11–24.5 109–697 1590–7130 2.77–12.0 b0.05 4.63–19.2 b0.02–0.56 b0.02–28.5 b0.02–1.18 b0.02–1.55 5.95–14.8 7.36–18.5 16.4–56.0 905–2560 271–807 1250–3940 2.96–19.9 2.79–13.8

16.3 12.5 1.27 30.9 355 6.19 1.76 8.41 b0.05 376 0.25 0.67 28.1 3290 0.35 57.6 13.1 239 3650 5.04 b0.05 8.27 0.04 0.14 0.05 0.29 8.70 11.8 29.2 1690 485 2430 5.70 5.08

19.1;37.6 12.8;30.7 1.79;4.21 36.1;70.2 8.66;25.2 1.44;1.54 0.81;1.64 5.80;13.6 b 0.05 25.4;33.3 b 0.02 b 0.02 b 0.05 18.6;48.8 0.05;0.11 0.82;1.43 0.04;0.66 1.84;4.62 21.3;55.6 b 0.10 n.a. 0.42;0.98 n.a. n.a. n.a. n.a. n.a. 7.81;8.68 n.a. 38.6;74.8 10.3;20.1 71.9;117 n.a. n.a.

26.8 19.8 2.75 50.3 14.8 1.49 1.15 8.89 b0.05 29.1 b0.02 b0.02 b0.05 30.1 0.07 1.08 0.16 2.92 34.4 b0.10

34.7;69.1 43.3;45.4 1.51;3.07 81.7;115 31.2;55.7 2.06;2.91 1.10;2.07 7.06;18.1 b0.05 41.5;78.8 b0.02 b0.02 b0.05 51.0;107 b0.02;0.12 1.83;2.48 0.04;1.29 7.92;8.26 61.4;119 b0.10 n.a. 1.17;1.47 n.a. n.a. n.a. n.a. n.a. 7.97;9.96 n.a. 75.0;153 19.7;49.6 116;238 n.a. n.a.

0.64

8.23 53.8 14.4 91.7

GM 49.0 44.4 2.15 97.1 41.7 2.45 1.51 11.3 b0.05 57.1 b0.02 b0.02 b0.05 73.9 0.03 2.13 0.23 8.09 85.4 b0.10 1.31

V. Savinov et al. / Science of the Total Environment 409 (2011) 2734–2745

α-HCH β-HCH γ-HCH ΣHCHa Oxychlordane Trans-chlordane Cis-chlordane Trans-nonachlor Heptachlor ΣCHLb α-Endosulfan β-Endosulfan o,p′-DDE p,p′-DDE o,p′-DDD p,p′-DDD o,p′-DDT p,p′-DDT ΣDDTc Endrin Methoxychlor Mirex 1.3.5 TCB 1.2.4 TCB 1.2.3 TCB 1.2.3.4 TetraCB PentaCB HCB ΣCBzd Σ10PCBe Σplanar PCBf ΣPCBg Parlar 26 Parlar 50

Kalgalaksha Bay, White Sea

8.91 107 31.2 166

(continued on next page)

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Table 2 (continued) POPs

Kalgalaksha Bay, White Sea

Vaygach Island, Barents Sea

Dikson Island, Kara Sea — Yenisei estuary

Female, N = 9

Female, N = 2

Female, N = 3

Range

a b c d e f g h i j k

b0.01–4.81 4.09–141 0.03–0.28 3.08–12.0 0.21–1.01 0.17–0.78 0.09–0.32 0.08–0.20 b0.01 3.71–13.2 b7.0–13.0 1.67–3.87 b0.4 b0.4 b0.4 b0.4–3.60 b0.4–7.95 5.57–19.8 22.8–40.7 0.66–1.93 3.57–6.21 b0.4–3.01 b0.4–1.34 b0.4–2.67 b0.4–2.35 b0.4–3.48 b0.4 b0.4–2.62 31.6–62.0 4.41–85.0 5.17–14.7 3.63–6.96 89.1–94.8

GM 0.69 11.4 0.11 6.00 0.49 0.41 0.18 0.12 b 0.01 7.48 6.42 2.59 b 0.4 b 0.4 b 0.4 0.52 1.28 12.5 30.9 1.11 4.34 0.84 0.49 0.71 0.66 0.85 b 0.4 0.50 42.2 16.7 9.35 4.81 92.1

Range b 0.01–1.97 5.07–31.9 0.02–0.16 4.35–9.64 0.22–0.99 0.16–0.55 0.11–0.35 0.06–0.14 b 0.01 5.82–11.6 b 7.0–21.1 1.35–2.94 b 0.4 b 0.4 b 0.4 b 0.4–3.07 b 0.4–25.6 8.59–33.2 19.1–43.0 b 0.4–1.65 2.31–6.30 b 0.4–3.57 b 0.4–1.28 b 0.4–2.87 b 0.4–2.87 b 0.4–25.78 b 0.4 b 0.4–2.12 24.0–75.0 3.72–28.2 5.40–22.5 2.70–7.24 86.6–95.0

GM 0.80 11.1 0.11 6.39 0.49 0.35 0.16 0.10 b0.01 7.70 10.0 2.06 b0.4 b0.4 b0.4 0.48 1.50 17.5 32.2 0.73 3.43 0.48 0.35 0.44 0.46 0.67 b0.4 0.42 42.5 6.32 12.4 4.59 90.6

Range 0.77;1.43 3.64;6.56 0.22;0.96 5.68;23.5 0.11;0.34 0.27;1.40 0.08;0.15 0.07;0.11 b 0.01 6.43;26.5 b 7.0 b 0.8 b 0.4 0.22;2.69 b 0.4 b 0.4;1.55 0.83;1.97 1.71;12.7 7.67;7.88 b 0.4;0.57 0.86;2.08 b 0.4 b 0.4 b 0.4 b 0.4 b 0.4 b 0.4 b 0.4 9.40;11.2 2.58;8.82 0.46;6.72 1.05;1.45 89.0;99.6

Male, N = 6 GM 1.05 4.89 0.46 11.6 0.19 0.62 0.11 0.09 b 0.01 13.1 b 7.0 6.43 b 0.4 0.77 b 0.4 0.58 1.28 4.65 7.77 0.35 1.34 b 0.4 b 0.4 b 0.4 b 0.4 b 0.4 b 0.4 b 0.4 10.3 4.77 1.76 1.23 94.2

Range 0.51–1.93 2.73–9.98 0.24–0.54 2.91–15.3 0.13–0.39 0.23–0.76 0.06–0.12 0.04–0.12 b0.01 3.65–17.1 b7.0 1.68 b0.4 0.21–1.11 b0.4 b0.4–0.48 b0.4–3.18 1.07–4.35 5.41–11.2 b0.4–0.59 0.75–2.48 b0.4–0.52 b0.4 b0.4 b0.4 b0.4–0.75 b0.4 b0.4–1.19 7.12–15.5 2.07–4.68 0.45–1.47 0.80–1.91 84.7–91.0

GM 1.13 5.59 0.36 8.29 0.20 0.41 0.10 0.07 b0.01 9.51 b7.0 b0.8–1.45 b0.4 0.32 b0.4 0.24 0.83 2.51 7.49 0.30 1.21 0.28 b0.4 b0.4 b0.4 0.26 b0.4 0.29 10.1 3.21 0.79 1.17 88.3

Range 1.25–5.81 7.22–28.1 0.11–0.67 3.85–15.3 0.05–0.30 0.10–0.95 0.03–0.18 0.02–0.15 b0.01–0.02 4.16–17.5 b7.0 0.75 b0.4 0.89–3.55 b0.4–1.25 b0.4–1.30 0.66–3.15 3.32–14.3 7.11–13.3 b0.4–0.92 0.98–5.26 b0.4 b0.4 b0.4 b0.4 b0.4 b0.4 b0.4 9.05–14.9 4.94–9.66 0.58–5.55 1.10–2.45 88.0–93.0

Vankarem, Chukotka Peninsula

Male, N = 3 GM 2.71 14.3 0.31 8.50 0.15 0.38 0.09 0.07 0.01 9.54 b7.0 b0.8–5.05 b0.4 1.43 0.42 0.43 1.45 5.65 9.17 0.38 1.82 b0.4 b0.4 b0.4 b0.4 b0.4 b0.4 b0.4 12.6 6.29 1.81 1.64 91.0

ΣHCH = sum of α-, β-, and γ-HCH. ΣCHL = sum of oxychlordane, trans-chlordane, cis-chlordane, trans-nonachlor, cis-nonachlor and heptachlor. ΣDDT = sum of o,p′-DDE, p,p′-DDE, o,p′-DDD, p,p′-DDD, o,p′-DDT, and p,p′-DDT. ΣCBz = sum of tri-, tetra-, penta- and hexa-CBz. Σ10PCB = sum of PCB28, 31, 52, 101, 105, 118, 138, 153, 156, and 180. Σ(n, m-o)PCB is sum of non- and mono-ortho substituted congeners of PCB: PCB77, 126, 169, 81, 105, 114, 118, 123, 156, 157, 167, 170, 180, and 189. ΣPCB = sum of 56 PCB congeners. ΣPBDE = sum of PBDE28, 47, 99, 100, 153, 154, and 183. ΣPCDD = sum of tetra-, penta-, hexa-, hepta-, and octa-CDD. ΣPCDF sum of tetra-, penta-, hexa-, hepta-, and octa-CDF. Calculated according to Van den Berg et al. (2006); n.a. = not analysed.

Range 0.61–3.37 6.36–37.1 0.13–0.50 8.46–19.7 0.15–0.34 0.32–1.47 0.07–0.16 0.04–0.21 b0.01 9.52–22.3 b7.0 1.59 b0.4 0.70–5.06 b0.4–0.83 0.20–0.85 1.30–2.63 2.80–21.4 5.80–8.24 b0.4–1.11 0.70–2.53 b0.4 b0.4–0.97 b0.4 b0.4 b0.4–0.78 b0.4 b0.4 9.20–11.2 6.77–20.4 0.49–12.9 1.03–1.48 87.4–92.5

Female, N = 2 GM 1.37 12.3 0.30 11.9 0.20 0.56 0.09 0.09 b 0.01 13.2 b 7.0 b 0.8–12.3 b 0.4 1.94 0.50 0.48 1.81 8.07 7.23 0.60 1.22 b 0.4 0.34 b 0.4 b 0.4 0.32 b 0.4 b 0.4 10.3 10.9 2.85 1.22 90.1

Range n.a. n.a. b 0.01 0.15;0.16 b 0.01 b 0.01;0.02 b 0.01 b 0.01 b 0.01 0.16;0.17 b 1.0 2.55 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2;0.87 b 0.2;0.57 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2;1.44 0.24;0.44 b 0.1 b 0.1;0.20 91.4;92.2

Male, N = 2 GM

Range

b 0.01 0.15 b 0.01 0.01 b 0.01 b 0.01 b 0.01 0.16 b 1.0 b 0.1 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 0.42 0.34 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 0.54 0.32 b 0.1 0.14 91.8

n.a. n.a. b0.01;0.07 0.14;0.44 b0.01 0.04 b0.01 b0.01 b0.01 0.17;0.61 b1.0 b0.1 b0.2 b0.2 b0.2 b0.2 b0.2 b0.2 2.80;4.05 0.65;1.82 b0.2;0.46 b0.2;0.32 b0.2 b0.2 b0.2 b0.2;0.46 b0.2 b0.2 4.22;6.33 0.45;1.26 b0.1 0.34;0.60 92.5;92.6

GM

0.03 0.25 b 0.01 0.09 b 0.01 b 0.01 b 0.01 0.32 b 1.0 b 0.1 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 3.37 1.09 0.30 0.25 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 b 0.2 5.17 0.75 b 0.1 0.45 92.6

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Parlar 62 ΣParlars PBDE#28 PBDE#47 PBDE#99 PBDE#100 PBDE#153 PBDE#154 PBDE#183 ΣPBDEh 2,3,7,8-TeCDD 1,2,3,7,8-PeCDD 1,2,3,4,7,8-HxCDD 1,2,3,6,7,8-HxCDD 1,2,3,7,8,9-HxCDD 1,2,3,4,6,7,8-HpCDD OCDD ΣPCDDi 2,3,7,8-TeCDF 1,2,3,7,8-PeCDF 2,3,4,7,8-PeCDF 1,2,3,4,7,8-HxCDF 1,2,3,6,7,8-HxCDF 2,3,4,6,7,8-HxCDF 1,2,3,7,8,9-HxCDF 1,2,3,4,6,7,8-HpCDF 1,2,3,4,7,8,9-HpCDF OCDF ΣPCDFj TEQPCBk TEQPCDDk TEQPCDFk Lipid, %

Male, N = 15

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usage for the control of disease vector populations in the basins of the rivers inflowing to the Kara Sea (Li et al., 2006). In ringed seals from all four areas studied, p,p′-DDE was the most abundant DDT compound, contributing 69.6% (Kalgalaksha Bay) to 87.1% (Vaygach Island) of ΣDDT concentrations. The highest contribution of parent DDT compound p,p′-DDT in ΣDDT (25.8%) was found for ringed seals from Kalgalaksha Bay while from the other three areas, this value ranged from 7.7% to 9%. This may indicate more fresh input of DDT to the White Sea ecosystem compared to the other three areas studied. ΣDDT residue levels in ringed seals from Kalgalaksha Bay and Vaygach Island were similar to those found in ringed seals from W Greenland (Johansen et al., 2004; Vorkamp et al., 2004) and selected areas of Canadian Arctic (Muir et al., 1999; de Wit et al., 2004; Mallory et al., 2005) but lower as compared to ringed seals from NW and NE Greenland (de Wit et al., 2004; Vorkamp et al., 2004). However ΣDDT levels in ringed seals from Kalgalaksha Bay and Vaygach Island were higher by comparison with ringed seals from Alaska (Hoekstra et al., 2003; Kucklick and Krahn, 2002; Krahn et al., 1997), and Labrador (Muir et al., 1999). ΣDDT levels in the blubber of ringed seal from Vankarem (54.2 ng/g lw) was greatly lower in comparison with the other compared Arctic areas and was quite similar to those found in 2001 in the ringed seals from the adjacent site at Chukotka Peninsula (66 ng/g lw) (AMAP, 2004). The ΣDDT concentrations in the blubber of ringed seals from the Kara Sea (Dikson) were two-fold lower compared with the 1995 data reported by Nakata et al. (1998) (3280 ng/g lw on average for male and female animals). However, the results for Dikson remained higher in comparison with other Arctic regions, keeping the trend of the regional distribution of this contaminant in Arctic ringed seals (de Wit et al., 2004). 3.1.3. PCBs In the former Soviet Union, mass production of technical PCB mixture Sovol (analogous of Aroclor 1254) and various mixtures of Sovol and trichlorobenzenes (Sovtol) began in 1939 (Ivanov and Sandell, 1992). Russia discontinued the production of PCB in 1992 (AMAP, 2000). Until that time, total production of three main PCB brands (Sovol, Sovtol and trichlorodiphenyl) was estimated to be 180,000 tonnes (Treger and Rozanov, 2000). An inventory of use in Russia to the late 1990s, estimated that approximately 27,000 tonnes of PCB was still in circulation in PCB-containing equipment (AMAP, 2000). Ranges of total concentrations of PCBs (ΣPCB = sum of 56 PCB congeners) found in the blubber of seals from Kalgalaksha Bay, Vaygach Island, Dikson Island, and Vankarem were 579–2420 ng/g lw, 614–1490 ng/g lw, 644–3940 ng/g lw, and 72–238 ng/g lw, respectively. Significantly higher geometric mean ΣPCB concentration was found in seals from Dikson Island (1540 ng/g lw). However this value was two-fold lower than those found in ringed seal from the same area in 1995 (Nakata et al., 1998). The observed rate of decline is similar to that found by Addison and Smith (1998) for ringed seals from Holman in the Western Canadian Arctic for the period 1972 to 1981 (38% for ΣDDT and 66% for ΣPCB) who attributed to the rapid decline to the control of DDT and PCB use in North America in the 1970s. Similar declines in the 1990s may reflect reductions in emissions of DDT and PCBs to the aquatic environment of northwest Russia during the late 1980s and early 1990s. For example, ΣDDT concentrations in the Severnaya Dvina River, which flows into Dvina Bay (White Sea), showed a 50% decline from 1988 to 1991 and declines were also found in other north flowing rivers in Russia during that time period (Zhulidov et al., 2000). There were no significant differences between ΣPCB concentrations found in the blubber of ringed seals from Kalgalaksha Bay (1080 ng/g lw) and Vaygach Island (838 ng/g lw). ΣPCB levels in ringed seal blubber from Kalgalaksha Bay were lower compared to

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those found in Dvina Bay (White Sea) in 1998 (1500 ng/g lw) (Muir et al., 2003). Significantly lower ΣPCB concentrations were found in ringed seals from Vankarem (124 ng/g lw). These values were quite similar to ΣPCB concentrations in ringed seal blubber collected in 2001 from a nearby sampling site in Chukotka Peninsula (AMAP, 2004). In general, results for PCBs in ringed seals from the Russian Arctic were in agreement with previously observed geographical trends in ΣPCB concentrations with levels being lowest in ringed seals from the Chukotka Peninsula, and highest in seals from the south-western Kara Sea (Muir et al., 2000; de Wit et al., 2004). However, ΣPCB concentrations in ringed seals from Svalbard reported by Kleivane et al. (2000) were 2 times higher than in ringed seals from Kalgalaksha Bay and Vaygach Island and similar to those found in ringed seals from Dikson Island. PCBs #153, #138/158, #99 and #118/149 were the most abundant congeners in the blubber of seal from all four areas studied; their totally relative amount ranged from 49% to 63% of ΣPCB. The observed PCB patterns were very similar to patterns in seals from other studies (Muir et al., 1988; Luckas et al., 1990; Wolkers et al., 1998 etc.), suggesting a similar biotransformation capacity. Geometric mean concentrations of dioxin-like PCBs (sum of nonand mono-ortho substituted PCBs), (Σ(n-,m-o)PCB = sum of PCB #PCB77, 126, 169, 81, 105, 114, 118, 123, 156, 157, 167, 170, 180, and 189) in blubber of seals from Vaygach Island, Kalgalaksha Bay, Dikson Island, and Vankarem were 150, 223, 378 ng/g lw, and 21.2 ng/g lw respectively. Sum of these PCB compounds contributed from 17% to 25% to ΣPCB. Kostamo et al. (2000) reported that the PCB congener composition in ringed seal blubber from the White Sea resembled a mixture of Aroclor 1254 and 1260. However our studies have shown that patterns of dioxin-like PCBs found in ringed seals from all four areas studied were quite similar to Aroclor 1254 (Schwartz et al., 1993) and the analogous Sovol (Kannan et al., 1992) produced in the former Soviet Union (Fig. 2). Geometric means of TCDD-toxic equivalent of dioxin-like PCBs (TEQPCB) calculated with toxic equivalency factors (TEFs) updated in 2005 (Van den Berg et al., 2006), (ranged from 0.50 pgTEQ/g lw (ringed seals from Vankarem) to 9.32 pgTEQ/g lw (Kalgalaksha Bay)) (Table 2). Only limited data exist on TEQPCB levels in ringed seals from the different Arctic areas (Nakata et al., 1998; Helm et al., 2002; Ikonomou, 2002; Amirova et al., 2004; Addison et al., 2005), however it is difficult to compare them with presented data due to great differences between TEFs for marine mammals which have been used before (Van den Berg et al., 1998) and are in use after 2005 (Van den Berg et al., 2006). For comparison, our data obtained for ringed seals from Dikson Island in 2002 and Vankarem in 2005 with data reported by Nakata et al. (1998) and Amirova et al. (2004) we have recalculated TEQPCB values using ‘old’ TEFs. The comparison showed that TEQPCB in blubber ringed seals from Dikson Island decreased from 160 pgTEQ/g lw in 1995 (Nakata et al., 1998) to 38.6 pgTEQ/g lw in 2002 and from 24.9 pgTEQ/g lw in 2001 (Amirova et al., 2004) to 2.1 pgTEQ/g lw in 2005 in the blubber of ringed seals from Chukotka Peninsula. 3.1.4. Chlordanes Technical chlordane is a mixture of at least 120 compounds, with the major constituents being cis- and trans-chlordane, heptachlor, cisand trans-nonachlor and others (Howard, 1991). Chlordane is a broad-spectrum contact insecticide that was employed on agricultural crops, for the control of termites, cockroaches, ants and other household pests (UNEP, 2002). The U.S. was the major world producer and user of chlordane, however there was limited use in Western Europe and former Soviet Union (UNEP, 2002). Total concentrations of chlordane-related compounds (ΣCHL = sum of oxychlordane, trans-chlordane, cis-chlordane, trans-nonachlor and heptachlor) in seal blubber were found in a wide range of

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V. Savinov et al. / Science of the Total Environment 409 (2011) 2734–2745

Fig. 2. Non- and mono-ortho substituted PCB patterns in blubber of ringed seals from the Russian Arctic and in technical PCB mixture Aroclor 1254 (Schwartz et al., 1993).

concentrations: from 6.46 ng/g lw up to 896 ng/g lw (Table 2). Significantly higher geometric mean ΣCHL concentrations (219 ng/g lw) were found in ringed seals from Dikson Island. Significantly lower ΣCHL concentrations were found in ringed seals from Kalgalaksha Bay (32.2 ng/g lw) and Vankarem (40.8 ng/g lw). Oxychlordane, which is formed from the metabolism of several chlordane isomers, was the most abundant in seals from all four areas studied. Higher contributions of oxychlordane in ΣCHL residue levels (94 to 98% of ΣCHL) in ringed seals from Kalgalaksha Bay, Vaygach Island and Dikson Island indicate a high extent of metabolic alteration of chlordane-related compounds while lower relative amounts of this pollutant in ringed seals from Vankarem (67%) probably indicates recent introductions of chlordane into the Chukchi Sea ecosystem. A comparison of present data with the results of previous studies conducted in the same areas showed that ΣCHL concentrations in ringed seals from the White Sea found in 1998 (Muir et al., 2003) and Kara Sea in 1995 (Nakata et al., 1998) decreased by more than 2-fold but remained on the same level as in ringed seals from the Chukotka Peninsula in 2001 (AMAP, 2004).

3.1.5. HCHs Hexachlorocyclohexanes (HCHs) are a group of related isomers exiting in eight isomeric forms. As an insecticide, HCH was available in two formulations: technical HCH containing 55–80% α-HCH, 8–15% γHCH, 5–14% β-HCH, and other isomers (Willett et al., 1998) and lindane containing almost pure insecticidal isomer γ-HCH. Total usage of HCH isomers in former Soviet Union from 1950 to 1990, when these pesticides were officially banned for agricultural use, was estimated to be 270,000 tonnes for γ-HCH, 1,270,000 tonnes for α-HCH and 170,000 tonnes for β-HCH (Li et al., 2005). The highest concentration of ΣHCHs (sum of α-, β- and γ-HCH) was found in the blubber of ringed seals from Vankarem. This apparently reflects high contamination of the Chukchi Sea ecosystem

by HCH isomers as a result of their transport from east Asian regions (Li, 1999) via atmospheric and marine pathways. Geometric mean of total concentrations of ΣHCH measured in tissues of seals from Vankarem (69.9 ng/g lw) was significantly higher as compared to those found in seals from the three other areas studied. The proportion of α-HCH in ΣHCH concentrations ranged from 53 to 64% (Fig. 3). However HCH patterns in ringed seals from Vankarem differed from other locations, with higher relative amount of β-HCH (44% of ΣHCH) that is the most toxicologically significant HCH isomer due to highly persistence in mammalian tissues (Willett et al., 1998). ΣHCH concentrations in ringed seals from Dikson Island were more than three times lower than reported in previous samples collected in 1995 (Nakata et al., 1998) was found. In contrast, ΣHCH concentrations in ringed seals from Kalgalaksha Bay and Vankarem, remained approximately the same as it was reported for samples collected in 1998 (White Sea) (Muir et al., 2003) and in 2001 (Chukotka Peninsula) (AMAP, 2004), respectively. Generally, ΣHCH levels, detected in seals from the Russian Arctic were 3–7 times lower compared to those in ringed seals from Alaska (Krahn et al., 1997; Kucklick and Krahn, 2002; Hoekstra et al., 2003), Greenland (Cleeman et al., 2000; Johansen et al., 2004; Vorkamp et al., 2004), Svalbard (Muir et al., 2000; de Wit et al., 2004), and from Canadian Arctic (Muir et al., 1999; Addison et al., 2009). 3.1.6. Chlorobenzenes Chlorobenzenes are produced as by-products in the production of a large number of chlorinated compounds such as chlorinated solvents and several pesticides (Bailey, 2001). Hexachlorobenzene (HCB) also had limited used in 1960s as a fungicide (de March et al., 1998). Total chlorobenzene concentration (ΣCBz = sum of 1,3,5-TCB, 1,2,4-TCB, 1,2,3-TCB, 1,2,3,4-TetraCB, 1,2,3,5-Tetra CB, 1,2,4,5-TetraCB, Penta CB and HCB) in the blubber of seals from Kalgalaksha Bay, Vaygach Island and Dikson Island ranged from 11.7 to 61.0 ng/g lw (Table 2).

Fig. 3. HCH patterns in the blubber of ringed seals from the Russian Arctic.

V. Savinov et al. / Science of the Total Environment 409 (2011) 2734–2745

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Fig. 4. Relative amounts of chlorobenzenes (% of ΣCBz) in the blubber of ringed seals from the Russian Arctic.

Although there were no significant differences between geometric means ΣCBz concentrations found in seals from these three areas studied chlorobenzene patterns differed (Fig. 4). In tissues of seals from Dikson and Vaygach Islands, HCB and PentaCB were the most abundant chlorobenzene compounds; their total contributions in ΣCBz were 95 and 78% respectively. However, in the blubber of seals from Kalgalaksha Bay the relative amount of these contaminants was 44% only whereas the total contribution of trichlorobenzenes was more than 50%. Trichlorobenzenes (1,2,4and 1,2,3-substituted) were detected in effluent from pulp mills, iron and steel manufacturing plants and municipal water pollution control plants (OME, 1988, 1991a,b,c). All listed here sources of trichlorobenzene contamination are present in the White Sea area in contrast to poor industrialised coastal areas of south-east Barents Sea and Kara sea. HCB was the only chlorobenzene compound detectable in the blubber of ringed seals from Vankarem. Geometric mean HCB concentration found in ringed seals from this area (8.6 ng/g lw) was significantly lower as compared with those found in ringed seals from the other three areas studied (10.5–12.8 ng/g lw) and quite similar to those found in ringed seals from the adjacent site at the Chukotka Peninsula in 2001 (AMAP, 2004). In the blubber of ringed seals from

Dikson Island, HCB concentration found in 2002 was two-fold lower compared samples collected there in 1995 (Nakata et al., 1998). HCB residue levels in ringed seals from Russian Arctic were similar to those found in ringed seals from Greenland (Johansen et al., 2004; Vorkamp et al., 2004), Hudson Strait and northern Labrador (Muir et al., 1999) but lower than in ringed seals from the western Canadian Arctic and Alaska (Krahn et al., 1997; Muir et al., 2000; Hoekstra et al., 2003) (Fig. 5). 3.1.7. Mirex Mirex concentrations in ringed seal blubber from the studied areas ranged from b0.05 to 19.2 ng/g lw (Table 2). Significantly higher geometric mean concentration (4.75 ng/g lw) was found in seals from Dikson Island. In the White Sea ringed seals, concentration of this pesticide did not exceed the MDL in all samples analysed, while in samples of 1998, mirex concentration was 8.8 ng/g lw (Muir et al., 2003). A two-fold decrease of mirex was found for ringed seals from Chukotka Peninsula as compared with 2001 (AMAP, 2004). In general, contamination levels of both, HCB and Mirex, in the blubber of ringed seals from Russian Arctic are comparable to those found in ringed seals from Greenland (Johansen et al., 2004; Vorkamp et al., 2004) but noticeably or greatly lower than in ringed seals from

Fig. 5. Circumpolar distribution of HCB and mirex (ng/g lipid weight) in the blubber of ringed seals (AMAP, 2004; Hoekstra et al., 2003; Krahn et al., 1997; Kucklick and Krahn, 2002; Mallory et al., 2005; Johansen et al., 2004; Muir et al., 1999; Vorkamp et al., 2004 and present data).

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Alaska (Krahn et al., 1997; Kucklick and Krahn, 2002; Hoekstra et al., 2003) and selected sites of the Canadian Arctic (AMAP, 2004; Hoekstra et al., 2003; Muir et al., 2000; Mallory et al., 2005) (Fig. 5). 3.1.8. Methoxychlor and endrin Methoxychlor was detected in ringed seal from Kalgalaksha Bay only at very low levels (b0.5–8.36 ng/g lw) and was less than the method detection limit (b0.05 ng/g) in ringed seals from the others three studied areas (Table 2). Endrin was found in ringed seal from Kalgalaksha Bay, Vaygach Island and Dikson Island. There were no statistically significant differences in geometric mean endrin concentrations in seals from Vaygach Island (2.03 ng/g lw) and Dikson Island (5.64 ng/g lw) whereas these values were significantly higher compared to those found in ringed seals from Kalgalaksha Bay (0.14 ng/g lw) (Table 2). 3.1.9. Toxaphene Toxaphene is the common name of complex mixture of chlorinated bornanes that was widely used as a pesticide in the US, Canada and other countries prior to its ban in the 1980s due to its environmental persistence and toxicity (Saleh, 1991). In the former Soviet Union, use of toxaphene has been severely restricted since 1992 (de March et al., 1998) but a large amount of wastes from production remain (UNEP, 2002). Toxaphene congeners were found in all blubber samples of ringed seals from Kalgalaksha Bay, Vaygach Island and Dikson Island. Total toxaphene concentrations (sum of Parlar 26, Parlar 50 and Parlar 62) ranged from 2.73 to 141 ng/g lw. Geometric mean blubber concentrations of these pesticides in ringed seals from Kalgalaksha Bay, Vaygach Island and Dikson Island were 11.2, 5.41 and 13.3 ng/g lw, respectively (Table 2). Due to great range of concentrations, there were no significant differences between them, however, toxaphene

patterns differed. Parlar 50 prevailed in the blubber of ringed seals from Kalgalaksha Bay and Vaygach Island, while Parlar 26 was the major toxaphene congener in seals from Dikson Island (Table 2). Concentrations of Parlar 26 and Parlar 50 in blubber of ringed seals from Russian Arctic were quite similar to those found in ringed seals from Svalbard (Wolkers et al., 1998) and Nunavik (NE Canada) (Gouteux et al., 2005) but noticeably lower than in ringed seals from Alaska (Hoekstra et al., 2003), Greenland (Cleeman et al., 2000) and Canadian Arctic (Hudson Strait and Ellesmere Island) (Muir et al., 1997, 1999) (Fig. 6). 3.1.10. PBDEs PBDEs are persistent and potentially toxic in the marine environment, including Arctic ecosystems (de Witt, 2002; de Wit et al., 2006). PBDEs were not produced in Russia. During the period 2000–2004, 20 tonnes of penta-BDE and 74 kg of octa-BDEs were imported into Russia from USA, Israel, Belgium, Ukraine, India and other countries (ACAP, 2006, 2007). PBDEs were found in all samples analysed. Total PBDE concentrations (ΣPBDE = sum of PBDEs #28, 47, 99, 100, 153, 154 and 183) in the blubber of ringed seals from Kalgalaksha Bay, Vaygach Island and Dikson Island, ranged from 3.65 to 26.5 ng/g lw and averaged 7.61, 10.3 and 11.2 ng/g lw, respectively (Table 2). There were no found significant differences between geometric mean ΣPBDE concentrations in the blubber of seals from these three areas, however, ringed seals from Vankarem had significantly lower concentrations (0.23 ng/g lw); 30–50 times lower than in ringed seals from the other three areas. BDE-47 (2,2′,4,4′-tetraBDE) was the major PBDE congener in all the samples analysed. Its contributions into ΣPBDE concentration in ringed seal blubber were from 80 to 90%. The predominance of lowerbrominated BDEs suggests that technical mixtures like DE-71 or Bromkal 70-5DE are the source of contamination. BDE-47 and also

Fig. 6. Circumpolar distribution of Parlar 26 and Parlar 50 in the blubber of ringed seals (Muir et al., 1997, 1999; Wolkers et al., 1998; Cleeman et al., 2000; Hoekstra et al., 2003; Gouteux et al., 2005 and present data).

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BDE-99 are the predominant congeners in these technical mixtures, contributing ΣPBDE 39–45% and 50–47%, respectively (La Guardia et al., 2006). Circumpolar ΣPBDE distribution (de Wit et al., 2006, 2010) showed that levels of ΣPBDE in ringed seals from the continental European Arctic were similar or slightly higher than those found in ringed seals from Canadian Arctic (Ikonomou et al., 2005; Muir et al., 2007), Alaska (Quakenbush, 2007) and central western Greenland (Vorkamp et al., 2008), however, lower than in ringed seals from Svalbard (Sørmo et al., 2006) and East Greenland (Vorkamp et al., 2008). The lowest blubber ΣPBDE concentration was found for ringed seals from Vankarem. 3.1.11. PCDD/Fs Polychlorinated dibenzo-p-dioxins and furans (PCDD/Fs) occur as by-products of industrial processes or products of incomplete incineration of chlorine-containing materials such as polyvinyl chloride plastic and from smelting of metals and the production of iron and steel (de March et al., 1998; UNEP, 2002). Pulp and paper mills using chlorine in the bleaching process have been an important source to the environment of PCDD/Fs (Kuehl et al., 1987; Tarasova et al., 1997) and in particular of 2,3,7,8-tetraCDD (de March et al., 1998). PCDDs were found in all blubber samples of ringed seals from Kalgalaksha Bay and Dikson Island and in 7 of 8 samples of ringed seals from Vaygach Island. In contrast, in all samples of ringed seals from Vankarem, residue levels of this contaminant did not exceed the method detection limit (b0.4 pg/g lw) while in 2001, ΣPCDD concentration in the blubber of ringed seals from Chukotka Peninsula was reported to be 4.86 pg/g lw (AMAP, 2004). ΣPCDD blubber concentrations in ringed seals from Kalgalaksha Bay, Vaygach Island and Dikson Island ranged from b0.4 to 33.2 pg/g lw, and on average (geometric means) were 15.3, 2.93 and 6.75 pg/g lw, respectively (Table 2). Significantly higher ΣPCDD concentration was found in ringed seals from Kalgalaksha Bay. Tetra-CDD was a major PCDD congener (58% of ΣPCDD) in ringed seals from this area, while it was not found in the blubber of seals from three other studied areas (Fig. 7a). White Sea region is heavily industrialised compared with the

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other regions studied; a number metallurgical works and pulp and paper mills are located in this region. Absolute predominance of tetraCDD in PCDD composition suggests the main role of pulp and paper mills discharges in PCDD contamination of the sea. ΣPCDFs concentrations in the blubber of ringed seals from the studied areas ranged from b0.2 to 75.0 pg/g lw. Geometric means were 4.67, 1.19, 1.41 and 0.25 pg/g lw in ringed seals from Kalgalaksha Bay, Vaygach Island, Dikson Island and Vankarem respectively (Table 2). Penta-CDFs prevailed in all blubber samples analysed (Fig. 7b). ΣPCDF levels found in ringed seals from Vankarem in 2005 were more than an order of magnitude lower compared with those reported for samples collected in 2001 (AMAP, 2004). Geometric means of TCDD-toxic equivalents calculated for PCDD (TEQPCDD) and PCDF (TEQPCDF) ranged from b0.1 to 11.1 pgTEQ/g lw and 0.25 to 4.67 pgTEQ/g lw, respectively. The both highest values were found in the blubber of ringed seals from Kalgalaksha Bay (Table 2). Moreover in ringed seals from this area only, total TEQPCDD/F has exceeded TEQPCB (Table 2). Only limited data exist on TEQPCDD/F levels in ringed seals: TEQPCDD/F value reported by Amirova et al. (2004) for the blubber of ringed seals from Chukotka Peninsula collected in 2001 was 0.87 pgTEQ/g lw, this is three times higher as compared with the presented data (0.25 pgTEQ/g lw). 4. Conclusions This study has expanded and updated the information available on POPs in ringed seals in the Russian arctic. ΣPCB, ΣDDT, ΣHCH and ΣCHL levels found in the blubber of seals from Kalgalaksha Bay, Vaygach Island, Dikson Island and Vankarem are in line with earlier studies of circumpolar geographical trends in concentrations of these contaminants in Arctic ringed seals (Muir et al., 2000; de Wit et al., 2004). Ringed seals from European part of Russian Arctic, had higher levels of ΣDDT and ΣPCBs compared with the other Arctic regions, while concentrations of other organochlorine compounds were similar or lower than in seals from Svalbard, Alaska, Canadian Arctic and Greenland. Ringed seals from south-western part of the Kara Sea (Dikson Island — Yenisei estuary) are the most contaminated with

Fig. 7. PCDD (a) and PCDF (b) patterns in the blubber of ringed seals from the Russian Arctic.

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POPs as compared with those found in the other three areas of Russian Arctic and with Alaska and the Canadian arctic. Ringed seals from Chukotka Peninsula (Vankarem) were generally the least contaminated with POPs as compared with ringed seals from the other Arctic regions. This study provides the first data on levels of PBDEs in the blubber of seals from the European part of the Russian Arctic. Concentrations are slightly higher than in ringed seals from the Canadian Arctic, Alaska and western Greenland but lower compared to seals from Svalbard and eastern Greenland. Only limited information is available on the trend in concentrations of POPs in seals from the Russian arctic. The data for seals from the Kara Sea and White Sea showed a decline compared with samples collected in 1995–1998. Further studies would be useful to update these trends. The highest of found in ringed seals from Russian Arctic total TCDD-toxic equivalent both PCDD/F and PCB was found in the White Sea, probably, due to local contamination sources mainly pulp and paper and metallurgical industries. Acknowledgements This work was carried out as part of project funded by the AMAP Secretariat and the Nordic Council of Ministers. The authors are thankful to anonymous reviewers who provided useful comments to the drafts of the manuscript. References Addison RF, Smith TG. Trends in organochlorine residue concentrations in Arctic ringed seals from Holman NWT 1972–1991. Arctic 1998;51:253–61. Addison RF, Ikonomou MG, Fernandez MP, Smith T. PCDD/F and PCB concentrations in Arctic ringed seals (Phoca hispida) have not changed between 1981 and 2000. Sci Total Environ 2005;351–352:301–11. Addison RF, Muir DCG, Ikonomou MG, Harwood L, Smith TG. Hexachlorocyclohexanes (HCH) in ringed seal (Phoca hispida) from Ulukhaktok (Holman), NT: trends from 1978 to 2006. Sci Total Environ 2009;407:5139–46. Amirova Z, Kruglov E, Vlasov S, Loshkina E, Khalilov R. PCBs and PCDD/Fs distribution in tissues and organs of marine animals in Russian Arctic. Organohalog Compd 2004;66:1533–41. Arctic Contaminants Action Program (ACAP). ACAP project on Brominated Flame Retardants (BFRs) phase I: inventory of sources of BFRs in the Russian Federation; 2006. Available from: http://acap.4poyntzdezign.com/index.php. Arctic Contaminants Action Program (ACAP). Final report of phase I of the ACAP project on brominated flame retardants (BFRs). Phase I: inventory of sources and identification of BFR alternatives and management strategies. OsloAMAP report 2007:6. SFT report TA-2440/2008; 2007. 51 pp. Arctic Monitoring and Assessment Programme (AMAP). PCB in the Russian Federation: inventory and proposals for priority remedial actions. Executive summary of the report of phase 1: evaluation of the current status of the problem with respect to environmental impact and development of proposals for priority remedial actions of the multilateral cooperative project on phase-out of PCB use, and management of PCB-contaminated wastes in the Russian Federation. AMAP Report 2000, vol. 3; 2000. Arctic Monitoring and Assessment Programme (AMAP). Persistent toxic substances, food security and indigenous peoples of the Russian North. Final report. Oslo: AMAP; 2004. 192 pp. Arctic Monitoring and Assessment Programme (AMAP). P.O.Box 8100 Dep., N-032 Oslo, Norway; 2009. 83 pp. Available on www.amap.no. Bailey RE. Global hexachlorobenzene emissions. Chemosphere 2001;43:167–82. Bengtson JL, Hiruki-Raring LM, Simpkins MA, Boveng PL. Ringed and bearded seal densities in the eastern Chukchi Sea, 1999–2000. Polar Biol 2005;28:833–45. Carroll J, Savinov V, Savinova T, Dahle S, McCrea R, Muir DCG. PCBs, PBDEs and pesticides released to the Arctic Ocean by the Russian Rivers Ob and Yenisei. Environ Sci Technol 2008;42:69–74. Chapsky KK. The ring seal of western seas of the Soviet Arctic. The morphological characteristics, biology, and hunting production. Trans. Arctic. Inst. Chief Administration Northern Sea Route, Leningrad 1940;45:15–71. (In Russian). Cleeman M, Riget F, Paulsen GB, de Boer J, Dietz R. Organochlorines in Greenland ringed seals (Phoca hispida). Sci Total Environ 2000;245:103. de March BGE, de Wit CA, Muir DCG, Braune BM, Gregor DJ, Norstrom RJ, et al. Chapter 6 — Persistent organic pollutants. In: de March BGE, de Wit CA, Muir DCG, editors. AMAP assessment report: Arctic pollution issues. Oslo, Norway: Arctic monitoring and assessment programme; 1998. p. 183–371. 859 pp. de Wit CA, Fisk AT, Hobbs KE, Muir DCG, Gabrielsen GW, Kallenborn R, et al. AMAP assessment 2002: persistent organic pollutants in the Arctic. Oslo, Norway: Arctic Monitoring and Assessment Programme; 2004. 309 pp.

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