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Organochlorine Burdens in Harbour Seals from the German Wadden Sea Collected During Two Phocine Distemper Epizootics and Ringed Seals from West Greenland Waters
ISSN: 2161-0525
Journal of Environmental & Analytical Toxicology

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Organochlorine Burdens in Harbour Seals from the German Wadden Sea Collected During Two Phocine Distemper Epizootics and Ringed Seals from West Greenland Waters

Siebert U1*, Heidmann A2, Friedhoff N2, Kruse H2, Rigét F3, Adler S1 and Maser E2

1Institute of Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Foundation, Werftstr. 6, 25761 Büsum, Germany

2Institute for Toxicology and Pharmakology, University of Kiel, Brunswiker Strasse 10, 24105 Kiel, Germany

3National Environmental Research Institute, University of Aarhus, PO Box 358, DK-4000 Roskilde, Denmark

*Corresponding Author:
Ursula Siebert
Institute of Terrestrial and Aquatic Wildlife Research
University of Veterinary Medicine Hannover, Foundation
Werftstr. 6, 25761 Büsum, Germany
Tel: 49-511-8568158
Fax: 49-511-8568181
E-mail: [email protected]

Received October 19, 2011; Accepted February 13, 2012; Published February 15, 2012

Citation: Siebert U, Heidmann A, Friedhoff N, Kruse H, Rigét F, et al. (2012) Organochlorine Burdens in Harbour Seals from the German Wadden Sea Collected During Two Phocine Distemper Epizootics and Ringed Seals from West Greenland Waters. J Environment Analytic Toxicol 2:126. doi: 10.4172/2161-0525.1000126

Copyright: © 2012 Siebert U, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Abstract

Blubber and liver of harbour seals from the German Bight collected between 2001 and 2002 and ringed seals from West Greenland waters were investigated for hexachlorocyclohexane (α-, β- and γ-HCH), hexachlorobenzene (HCB), dichlorodiphenyltrichlorethane and its metabolites (DDT, DDE and DDD), and polychlorinated biphenyls (PCBs). In blubber and liver of both species PCBs 138 and 153 showed the highest concentrations, followed by PCBs 187, 180 and 170. With the exception of PCB 52, the PCB burden in liver and blubber of harbour seals was higher than in ringed seals but not always statistically significant. Compared to levels found in harbour seals from the first seal epidemic in 1988, individuals collected in 2002 showed a decrease in concentrations of organochlorines. These data show that ringed seals from arctic waters are exposed to as large a variety of organochlorines as harbour seals from the North
Sea.

Keywords

Organochlorines; Ringed seal; Harbor seal; Greenland; North Sea; German Wadden Sea

Introduction

Organochlorines such as hexachlorocyclohexane (α-, β- and γ-HCH), hexachlorobenzene (HCB), dichlorodiphenyltrichlorethane and its metabolites (DDT, DDE and DDD), and polychlorinated biphenyls (PCB) accumulate in the marine ecosystem as shown in several studies (reports of AMAP, UNEP, TMAP). Negative effects were demonstrated for most of those chemicals, resulting in a European ban of DDT in 1972 and of PCBs in 1989, and a worldwide ban in 2001 (www.chem.unep.ch/pops).

Marine mammals are at the top of the marine food chain and accumulate chemical pollutants in their tissues. Ringed seals (Phoca hispida) are widely distributed in arctic and subarctic waters [1,2]. They feed on fish and crustaceans (Parathemisto sp.) and give birth to their offspring on ice in the spring [3]. Harbour seals (Phoca vitulina) are the most common pinniped species in the Wadden Sea. They feed mainly on fish in the open North Sea and give birth on the sand banks of the Wadden Sea during the summer months [4]. Two epizootics caused by the phocine distemper virus (PDV) occurred among the harbour seal population of the Wadden Sea and adjacent waters [5-7]. These outbreaks resulted in the deaths of more than 23,000 harbour seals in 1988 and 30,000 in 2002 [8-10].

Negative effects of organochlorines have been described for different seal species. Stenosis/occlusion of the uterus, osteoporosis, colonic ulcera, splenic atrophy, and lymphocytic depletion in thymus and lymph nodes were found in grey and ringed seals from the Baltic Sea and harbour seals from the Wadden Sea [11-16]. Immunological investigations revealed that the impairment of the immune response by organochlorines increased the susceptibility to diseases caused by viruses such as phocine distemper virus [17,18]. Therefore, an effect on the occurrence of epizootics in the harbour seal populations of the North and Baltic Seas could not be ruled out [8].

The objective of this study was to compare findings from German harbour seals collected around the two PDV epizootics in 1988 and 2002 and to examine whether the banning of DDT and PCB has resulted in a decrease of the levels in seals. Concentrations of different organochlorines in seals from West Greenland waters, far from the industrialised areas in Europe and North America, were compared with those from the North Sea.

Materials and Methods

Sample collection

Harbour seals from the German waters were collected between June 2001 and October 2002 through the stranding network of Schleswig- Holstein. Blubber and liver samples were taken during routine post mortem examination conducted during monitoring programmes [19]. Results of 26 harbour seals for the comparison of PDV-positive and PDV-negative animals (Table 1: animals 1-26) and 20 harbour seals were included for the comparison between ringed and harbour seals (Table 1: animals 10-29).

Seal number Date of collection Location of collection Sex (m = male,
f = female)
Age
Years
North Sea Harbour seals (Phoca vitulina)        
1 13.09.2002 Eiderstedt f 1.25
2 05.05.2002 Helgoland f 1.0
3 06.09.2002 Eiderstedt m 0.25
4 15.09.2002 Eiderstedt m 0.25
5 18.09.2002 Eiderstedt f 1.25
6 18.09.2002 Eiderstedt f 1.25
7 19.09.2002 Eider-Wesselburen-Vollerwiek f 2.25
8 02.10.2002 Sylt m 5
9 02.10.2002 Sylt f 0.25
10 21.08.2002 Eiderstedt m 7
11 31.05.2002 Helgoland f 2
12 25.07.2002 Sylt m 6
13 29.08.2002 Eiderstedt f 1.25
14 02.09.2002 Eiderstedt m 1.25
15 29.08.2002 Ostsee m 2.25
16 04.06.2002 Eiderstedt f 0.1
17 11.07.2002 Amrum-Fohr-Dagebüll m 0.1
18 12.08.2002 Amrum-Fohr-Dagebüll m 1.25
19 19.07.2002 Helgoland m 1
20 15.08.2002 Helgoland m 4
21 03.09.2002 Eiderstedt m 13
22 02.09.2002 Amrum-Fohr-Dagebüll f 0.25
23 03.09.2002 Eiderstedt f 1.25
24 05.09.2002 Eiderstedt m 6
25 05.09.2002 Eiderstedt f 10
26 05.09.2002 Eiderstedt f 3
27 05.06.2001 Amrum-Fohr-Dagebüll f >1.5
28 11.06.2001 Sylt f 8
29 06.09.2002 Eiderstedt f 8
Greenland Ringed seals (Phoca hispida)        
30 24.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
31 24.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
32 24.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
33 24.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
34 24.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
35 24.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
36 28.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
37 28.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
38 28.04.2002 Qeqertarsuaq, Disko Fjord m 0.5
39 01.05.2002 Qeqertarsuaq, Disko Fjord m 0.5
40 24.04.2002 Qeqertarsuaq, Disko Fjord m 1.5
41 24.04.2002 Qeqertarsuaq, Disko Fjord m 1.5
42 01.05.2002 Qeqertarsuaq, Disko Fjord m 1.5
43 28.04.2002 Qeqertarsuaq, Disko Fjord m 3.5
44 01.05.2002 Qeqertarsuaq, Disko Fjord f 0.5
45 01.05.2002 Qeqertarsuaq, Disko Fjord f 0.5
46 28.04.2002 Qeqertarsuaq, Disko Fjord f 1,5
47 24.04.2002 Qeqertarsuaq, Disko Fjord f 2.5
48 24.04.2002 Qeqertarsuaq, Disko Fjord f 3.5
49 24.04.2002 Qeqertarsuaq, Disko Fjord f 4.5

Table 1: Date and location where ringed and harbour seals were collected, sex and age.

Blubber and liver samples of 20 ringed seals hunted by Inuits in Qeqertarsuaq, West Greenland were collected during April and May 2002. 14 ringed seals were males (all subadults) and 6 were females (2 adults and 4 subadults) (Table 1: animals 30-49).

All tissue samples were taken with stainless steel instruments, Greenlandic samples were placed in optically opaque glass jars and German samples were placed in aluminum foil and stored in a -18°C freezer until analysis. Because of limited sample size varying numbers of samples were available for individual PCB investigations.

Analysis of organochlorines

Standards for PCB congeners (IUPAC-no) 28, 52, 101, 118, 128, 138, 153, 170, 177, 180, 183, 187, 197, β-HCH, γ-HCH and 4,4-DDT solved in isooctane produced by Dr Ehrenstorfer, Augsburg, Germany, and for α-HCH, HCB, 4,4`-DDE and 4,4`-DDD produced by Riedel De Haen, Seelze, Germany, were used. PCB congener 112 from Dr Ehrenstorfer, Augsburg, Germany, was added as an internal standard. Acetone, n-hexane, isooctane and dichloromethane (SupraSolv) were purchased from Merck, Darmstadt, Germany.

Organochlorines were analysed as described by [20]. The samples were extracted by a microwave MSP 1000 (SP-19, CEM Corporation, Matthews, NC,USA). 0.5-1 g tissue sample into 100 ml microwave vessel, 10 ml acetone (SupraSolv, Merck, Darmstadt, Deutschland) and 10 ml internal standard. After 45 min samples were cooled to 24°C. Organochlorine compounds were separated with GC-ECD (Varian). The organochlorine concentrations were calculated on a lipid-weight basis (Varian Star Chromatography Workstation 5.31).

For statistical analysis of the data the statistical open source platform R version 2.9.2 (R Development Core Team 2009) was used.

Testing for significant differences between the pollution levels in liver and blubber of the harbour seals, distinguished for PDV-positive and PDV-negative, a T-test was applied for simplicity as the values were more or less symmetrically distributed around the mean. As the number of animals with both liver and blubber data available was low, the results must be viewed with caution.

For comparison of the harbour seals data of from seal die-off in 1988 [21] and in 2002, only the mean values of the pollutant levels for the 1988 data were available. Here, a one-sample T-test was used.

The effect of age on the pollutant levels was tested using a regression analysis between the single pollution level as response and age as predictor, applying a GLM using Poisson error distribution with a correction of the standard errors using a quasi-GLM with a second order polynomial for males and females separately in combination with a backward selection. The 5% level of statistical significance was selected.

When comparing the pollution levels between ringed and harbour seals and within each population between liver and blubber, a general linear model (GLM) was applied using Poisson error distribution with a correction of the standard errors using a quasi-GLM [22,23], as the variance is different between both populations and, as mentioned earlier, the sample size is low. With a larger sample size with comparable variance structure, a GLM with log normal distribution would have been used.

Results and Discussion

Comparison between harbour seals found around the two seal epizootics

Harbour seals were collected in and around the year 2002 when the second phocine distemper virus epizootic occurred [6,7]. 15 individuals were infected with phocine distemper virus as shown by PCR and immunocytochemistry [7]. Contrary to males, infected females showed higher concentrations of organochlorines in the liver than those who tested negative (Table 2, Figure 1). In liver tissue, the results were significant for DDE using a T-test (t = 2.93, p-value = 0.01, df = 10.99) and most of the PCBs (e.g. PCB 128: t = 2.49, p-value = 0.03, df = 10.081) congeners. In blubber tissue, however, results did not show significant differences. The correlation between PCBs concentrations and susceptibility to phocine distemper virus infections had been investigated through different research activities during the epizootics. [24] found higher organochlorine (OC) concentrations in the blubber of diseased harbour seals compared to those who survived the die-off. A feeding experiment showed that the immunosuppressive effect of PCBs increased the likelihood of mass mortalities due to viral infections [18].

environmental-analytical-toxicology-Comparison-harbour

Figure 1: Comparison of harbour seals with (pos) and without (neg) PDV infection subdivided by organ and sex (ng/g lipid weight). N = number, DDT = dichlorodiphenyltrichlorethane, HCH = hexachlorocyclohexane, PCB = polychlorinated biphenyls.

      blubber     liver  
pollutant sex neg pos p neg pos p
               
α-HCH all 5.64 (5.51; 11) 6.27 (2.78; 15) n.s. 0.13 (0.05; 4) 0.11 (0.08; 3) n.s.
  female 4.61 (3.7; 5) 7.13 (2.95; 8) n.s. 0.2 (-; 1) 0.2 (-; 1) -
  male 6.51 (6.91; 6) 5.29 (2.42; 7) n.s. 0.1 (0; 3) 0.07 (0.04; 2) n.s.
               
β-HCH all 35 (26.63; 3) 17.64 (7.88; 8) n.s. 0.43 (0.49; 3) 0.3 (0.14; 2) n.s.
  female 38 (-; 1) 19.25 (4.57; 4) - 1 (-; 1) 0.2 (-; 1) -
  male 33.5 (37.48; 2) 16.02 (10.82; 4) n.s. 0.15 (0.07; 2) 0.4 (-; 1) -
               
γ-HCH all 3.29 (2.92; 7) 4.25 (1.28; 8) n.s. 0.6 (0.82; 11) 0.81 (0.76; 15) n.s.
  female 4.67 (4.04; 3) 4.4 (1.52; 5) n.s. 0.46 (0.23; 5) 0.53 (0.28; 8) n.s.
  male 2.26 (1.69; 4) 4 (1; 3) n.s. 0.72 (1.13; 6) 1.14 (1.01; 7) n.s.
               
HCB all 2.46 (3.1; 7) 1.99 (2.68; 4) n.s. 9.16 (12.03; 7) 20.68 (43.37; 14) n.s.
  female 7 (0; 2) 2.43 (3.09; 3) n.s. 6 (4.55; 4) 10.19 (16.22; 8) n.s.
  male 0.65 (0; 5) 0.65 (-; 1) - 13.37 (18.89; 3) 34.67 (64.13; 6) n.s.
               
OCS all 0.04 (0; 2) 15 (27.46; 9) n.s. - 0.25 (0.07; 2) -
  female 0.04 (0; 2) 23.81 (35.88; 5) n.s. - - -
  male - 4 (1.83; 4) - - 0.25 (0.07; 2) -
               
DDD all 26.09 (23.1; 11) 35.67 (37.74; 15) n.s. 2.48 (2.78; 11) 6.73 (12.95; 15) n.s.
  female 34.2 (33.69; 5) 45.63 (50.57; 8) n.s. 2.26 (1.7; 5) 3.25 (2.25; 8) n.s.
  male 19.33 (6.25; 6) 24.29 (7.5; 7) n.s. 2.67 (3.61; 6) 10.71 (18.72; 7) n.s.
               
DDE all 1254.45 (974.21; 11) 1683.53 (1092.04; 15) n.s. 31.09 (23.96; 11) 153.07 (308.33; 15) n.s.
  female 1351 (1291.77; 5) 1820.38 (1452.1; 8) n.s. 23.2 (18.38; 5) 64.13 (31.92; 8) s.
  male 1174 (739.02; 6) 1527.14 (518.76; 7) n.s. 37.67 (27.63; 6) 254.71 (445.02; 7) n.s.
               
DDT all 105.45 (89.15; 11) 116.73 (57.81; 15) n.s. 2.05 (3.48; 6) 16.19 (28.94; 11) n.s.
  female 101.8 (73.86; 5) 114.63 (58.26; 8) n.s. 0.78 (0.87; 4) 5.58 (5.91; 7) n.s.
  male 108.5 (107.27; 6) 119.14 (61.85; 7) n.s. 4.6 (6.22; 2) 34.75 (44.72; 4) n.s.
               
PCB_101 all 419.27 (368.28; 11) 523.67 (363.32; 15) n.s. 8.64 (5.66; 11) 36.13 (56.62; 15) n.s.
  female 593 (498.81; 5) 617.13 (478.9; 8) n.s. 7.8 (6.26; 5) 20.5 (9.43; 8) s.
  male 274.5 (129.95; 6) 416.86 (124.42; 7) n.s. 9.33 (5.61; 6) 54 (81.72; 7) n.s.
               
PCB_118 all 110.91 (76.81; 11) 149.53 (95.87; 15) n.s. 2.47 (1.48; 10) 7.33 (8.52; 15) s.
  female 144 (102.53; 5) 176.88 (125.41; 8) n.s. 1.97 (1.26; 5) 4.63 (2.26; 8) s.
  male 83.33 (37.16; 6) 118.29 (30.97; 7) n.s. 2.96 (1.65; 5) 10.43 (11.93; 7) n.s.
               
PCB_128 all 511.09 (387.32; 11) 680.27 (405.52; 15) n.s. 11.73 (7.59; 11) 83 (188.5; 15) n.s.
  female 607.6 (519.37; 5) 667.13 (484.22; 8) n.s. 11 (8.97; 5) 25 (11.15; 8) s.
  male 430.67 (259.15; 6) 695.29 (331.17; 7) n.s. 12.33 (7.06; 6) 149.29 (270.47; 7) n.s.
               
PCB_138 all 5228.73 (4396.64; 11) 7680.87 (4914.99; 15) n.s. 148.45 (107.17; 11) 1066.47 (2352.5; 15) n.s.
  female 6250.6 (5975.8; 5) 8140.38 (5998.88; 8) n.s. 143.4 (136.11; 5) 341.75 (155.22; 8) s.
  male 4377.17 (2859.77; 6) 7155.71 (3712.02; 7) n.s. 152.67 (90.01; 6) 1894.71 (3374.11; 7) n.s.
               
PCB_153 all 6509.73 (5409.98; 11) 9872 (7003.68; 15) n.s. 163.73 (110.91; 11) 1340.47 (2981.11; 15) n.s.
  female 7747.2 (7206.37; 5) 10838.63 (8989.95; 8) n.s. 147.2 (128.34; 5) 397.75 (189.87; 8) s.
  male 5478.5 (3766.02; 6) 8767.29 (4182.69; 7) n.s. 177.5 (104.53; 6) 2417.86 (4260.89; 7) n.s.
    6) 7)     7)  
               
PCB_170 all 987.45 (836.67; 11) 1712.4 (1637.46; 15) n.s. 27.45 (21.2; 11) 257.2 (539.91; 15) n.s.
  female 1289.4 (1131.75; 5) 2134.38 (2132.86; 8) n.s. 29.4 (28.14; 5) 91.88 (60.9; 8) s
  male 735.83 (456.29; 6) 1230.14 (663.52; 7) n.s. 25.83 (16.08; 6) 446.14 (773.15; 7) n.s.
PCB_177 all 379.64 (293.34; 11) 648.07 (572.99; 15) n.s. 19.36 (15.45; 11) 112.13 (225.08; 15) n.s.
  female 489.6 (387.22; 5) 743.75 (753.64; 8) n.s. 24.6 (21.55; 5) 51.5 (39.55; 8) n.s.
  male 288 (173.14; 6) 538.71 (278.02; 7) n.s. 15 (7.46; 6) 181.43 (325.39; 7) n.s.
PCB_180 all 1435.27 (1165.68; 11) 2519.67 (2567.63; 15) n.s. 38.73 (25.94; 11) 361.8 (722.86; 15) n.s.
  female 1832.6 (1551.83; 5) 3212.25 (3390.98; 8) n.s. 38 (33.04; 5) 141.5 (101.12; 8) s.
  male 1104.17 (708.27; 6) 1728.14 (772.86; 7) n.s. 39.33 (21.71; 6) 613.57 (1033.75; 7) n.s.
PCB_183 all 308.82 (245.45; 11) 584.6 (525.04; 15) n.s. 8.87 (5.83; 11) 85.6 (180.8; 15) n.s.
  female 391.8 (323.26; 5) 675.38 (660.03; 8) n.s. 8.4 (7.44; 5) 32.13 (26.09; 8) s.
  male 239.67 (155.79; 6) 480.86 (333.83; 7) n.s. 9.27 (4.82; 6) 146.71 (259.44; 7) n.s.
PCB_187 all 1552.73 (1219.47; 11) 2637.47 (2219.62; 15) n.s. 83.45 (72.03; 11) 499.4 (997.21; 15) n.s.
  female 1928.4 (1544.03; 5) 3098.25 (2900.05; 8) n.s. 96.4 (96.74; 5) 206.13 (136.68; 8) n.s.
  male 1239.67 (899.04; 6) 2110.86 (1037.83; 7) n.s. 72.67 (50.82; 6) 834.57 (1432.75; 7) n.s.
PCB_194 all 158.27 (158.59; 11) 291.67 (396.52; 15) n.s. 3.71 (2.47; 11) 48.27 (91.63; 15) n.s.
  female 197.6 (204.16; 5) 357.88 (522.43; 8) n.s. 3.72 (3.21; 5) 21.13 (19.41; 8) s.
  male 125.5 (118.81; 6) 216 (189.52; 7) n.s. 3.7 (1.99; 6) 79.29 (130.56; 7) n.s.
PCB_28 all 19.07 (26.77; 2) - - - - -
  female 0.14 (-; 1) - - - - -
  male 38 (-; 1) - - - - -
PCB_52 all 116.45 (106.41; 11) 140.2 (102.67; 15) n.s. 2.34 (1.12; 8) 6.5 (6.98; 14) n.s.
  female 157.6 (143.79; 5) 161.25 (117.91; 8) n.s. 2.5 (1.29; 4) 4.29 (2.5; 7) n.s.
  male 82.17 (54.8; 6) 116.14 (84.31; 7) n.s. 2.18 (1.09; 4) 8.71 (9.38; 7) n.s.

Table 2: Levels of pollutants in PDV-positive (pos) and PDV-negative (neg) harbour seals separated for blubber and liver (ng/g lipid weight). Levels of pollutants were tested by T-test (s. significant, n.s. not significant) in blubber and liver. Given is the mean and in brackets the standard deviation with the number of available samples for each pollutant group.

Comparison between regions

All organochlorines analysed in the present study were found in seals from both areas (Table 4). In both species, hexachlorocyclohexane (α-, β- and γ-HCH), hexachlorobenzene (HCB), dichlorodiphenyltrichlorethane and its metabolites (DDT, DDE and DDD), and polychlorinated biphenyls (PCBs) were found. In blubber and liver of both species, PCBs 138 and 153 showed the highest concentrations, followed by PCBs 187, 180 and 170. The PCBs burden in blubber and liver of harbour seals was several times higher than in ringed seals (e.g., PCB 138) with the exception of PCB 52, which was highest in the liver of ringed seals. Levels of DDE and DDD were also higher in harbour seals (blubber – DDE: t = -7.94 p << 0.01, df = 37, DDD: t = -6.23 p << 0.01, df = 33) than in ringed seals, only DDT was higher in blubber of ringed seals (t = 2.61 p = 0.01, df = 35). α-, β-HCH and HCB in blubber were higher (e.g., α-HCH: t = 11.73 p << 0.01, df = 38) but in liver lower in ringed seals than harbour seals (e.g., HCB: t = -5.32 p << 0.01, df = 7). For γ-HCH concentrations, it was the opposite, with higher levels in liver of ringed seals (t = 2.81, p = 0.01, df = 13) and lower levels in blubber (t = -5.34, p << 0.01, df = 26). The variance within the ringed and harbour seals concerning the single pollutants was high (Table 4, e.g. PCB 52 or DDT). This could not be explained by the parameters of age or sex available in this study.

    blubber     liver  
pollutant mean n p mean n p
α-HCH 141 149 s. 2 149 s.
β-HCH 90 149 s. 1 149 s.
γ-HCH 34 149 s. 2 149 s.
HCB 27 149 s. 0,4 149 s.
OCS 49 149 s. 1 149 s.
DDD 202 149 s. 39 149 s.
DDE 4847 149 s. 155 149 n.s
DDT 2829 149 s. 75 149 s.
PCB_101 911 149 s. 23 149 n.s
PCB_118 NA - - - - -
PCB_128 1405 149 s. 12 149 n.s
PCB_138 13929 149 s. 1226 149 n.s
PCB_153 22971 149 s. 471 149 n.s
PCB_170 2241 149 s. 101 149 n.s
PCB_177 1713 149 s. 58 149 n.s
PCB_180 6735 149 s. 83 149 n.s
PCB_183 1201 149 s. 12 149 n.s
PCB_187 2717 149 n.s. 46 149 n.s
PCB_194 394 149 s. 3 149 n.s
PCB_28 - - - - - -
PCB_52 231 149 s. 4 149 n.s

Table 3: Mean values of pollutants for harbour seals 1992 [Vagts] (ng/g lipid weight), standard deviation is not available. The means were tested for significant differences by one-sample T-test with the data of 2002, the result is given in the column p; s. = significant different, n.s. = not significant different.

    ringed seals     harbour seals      
              blubber liver
  blubber liver sig diff blubber liver sig diff rs:hs rs:hs
α-HCH 75.38 (35.68; 20) 11.81 (5.65; 6) s. 6.13 (± 4.22; 20) 15.34 (± 6.17; 2) s. s. n.s
β-HCH 38.08 (23.34; 20) NA - 19.08 (± 16.99; 13) 159.66 (± 13.64; 2) n.s. s. -
DDD 2.16 (1.04; 17) 46.35 (±NA; 1) - 16.73 (± 15.7; 18) 174.17 (± NA; 1) - s. -
DDE 190.15 (76.16; 19) 131.72 (84.55; 13) s. 1487.3 (± 1103.31; 20) 1282.25 (± 831.94; 8) n.s. s. s.
DDT 74.17 (48.62; 17) 856.4 (1969.39; 14) n.s. 43.51 (± 48.07; 20) 1113.23 (± 910.22; 7) s. s. n.s.
γ-HCH 4.94 (2.63; 20) 522.53 (491.33; 10) s. 13.42 (± 10.59; 8) 59.64 (± 29.62; 5) s. s. s.
HCB 44.8 (137.95; 20) 33.77 (8.42; 6) s. 18.32 (± 59.1; 15) 216.39 (± 155.15; 3) n.s. n.s. s.
IS_OCS 26.98 (17.21; 19) NA - 2.87 (± 1.43; 6) NA - s. -
PCB_101 22.27 (12.53; 20) NA - 450.69 (± 417.33; 20) 363.26 (± 104.44; 5) n.s. s. -
PCB_112 NA 1879.65 (1625.52; 13) - 83.97 (± 14.48; 19) 2668.31 (± 1191.31; 7) s. - n.s.
PCB_118 23.33 (18.13; 20) 48.49 (2.86; 2) n.s. 41.11 (± 36.7; 20) NA - s.  
PCB_128 NA NA - 2945.87 (± 10817.42; 20) 741.7 (± 701.79; 4) n.s. - -
PCB_138 51.71 (19.86; 20) 63.86 (42.11; 7) n.s. 4276.75 (± 3221.9; 20) 8484.97 (± 11510.3; 8) s. s. n.s
PCB_153 89.41 (39.27; 20) 332.18 (619.82; 8) n.s. 5767.3 (± 5029.21; 20) 10681.63 (± 15667.64; 8) n.s. s. s.
PCB_170 5.98 (4.93; 20) 21.76 (±NA; 1) - 1129.09 (± 1329.68; 19) 1883.62 (± 2716.97; 7) n.s. s. n.s.
PCB_177 2.21 (±NA; 1) NA - 444.99 (± 339.27; 20) 830.92 (± 811.28; 8) s. n.s. -
PCB_180 21.91 (13.1; 18) 76.69 (31.73; 2) s. 1642.61 (± 1638.78; 19) 2381.71 (± 3702.93; 8) n.s. s. n.s
PCB_183 NA NA - 485.32 (± 447.49; 14) 876.76 (± 1079.77; 4) n.s. - -
PCB_187 13.11 (9.91; 16) NA - 1787.66 (± 1751.31; 20) 4087 (± 5684.59; 8) s. s. -
PCB_194 1.7 (0.95; 2) 69.52 (49.83; 3) n.s. 180.79 (± 237.47; 19) 463.74 (± 648.89; 7) s. n.s. n.s.
PCB_28 9.57 (5.29; 16) NA - 11.03 (± 3.68; 11) NA - n.s. -
PCB_52 11.95 (5.36; 20) 460.46 (681.25; 14) s. 146.02 (± 118.08; 20) 224.35 (± 149.6; 2) n.s. s n.s

Table 4: Comparison of pollution levels between ringed and harbour seals in liver and blubber (ng/g lipid weight). Given is the mean and in brackets the standard deviation with the number of available samples for each pollutant group. sig diff: comparison between pollution levels within the ringed seals and harbour seals using a paired T-test. When comparing the pollution levels between ringed seals and harbour seals (rs:hs) for liver and blubber (last two columns) a GLM was used.

Levels found in Greenlandic ringed seals from the west coast were similar to those in ringed seals from the same area of Greenland, Alaska and Canada [25-27]. But levels were lower than those in ringed seals originating from the east coast of Greenland, Norway and Svalbard [26,28,29].

Temporal trends

From 1988 to 1992, the burdens of PCBs and DDT in harbour seals from German waters increased [21,30]. But when comparing findings between 1988-1992 [21,30] and 2002 (this study), concentration levels of all pollutants decreased, e.g. α-HCH and DDT by the factor 20 (Table 3 and 4, p << 0.05). Unfortunally no data on PCB levels of harbour seals from German waters are available for the period between 1992 and 2001 explaining when the decrease in body burden started. The decline in the burdens of HCB, HCH, OCS, DDT and DDD was distinct and confirmed earlier investigations [30]. A decreasing input can thus be assumed after the banning of technical HCH mixtures in many countries. The concentrations of PCBs and DDE decreased less noticeably because they are more persistent in the marine food web. Those findings were also confirmed in 18 harbour seals found dead in the Dutch Wadden Sea during the second PDV epizootic in 2002 [31]. HCH and HCB levels showed a significant decline but PCBs, DDT and DDE did not decrease significantly.

In all investigations PCBs 138 and 153 showed the highest concentrations. In general, ‘legacy’ persistent organic pollutants (POP) in arctic biota has showed decreasing trends during the past two to three decades [32]. This has also been the case for West Greenland ringed seals. For example, the concentrations of PCBs and DDT showed an annual decrease of 6.1 and 8.1%, respectively, during the period 1994 to 2006 [27].

Sex and age ratio

Male and female ringed and harbour seals in this study did not show a significant difference in PCBs using a GLM for testing (e.g., PCB 101, ringed seals: t = -1.13, p = 0.28, df = 18; harbour seals: t = 0.62 p = 0.54, df = 18), DDT (ringed seals: t = -0.57, p = 0.58 , df = 18; harbour seals: t = -0.89, p = 0.39, df = 18) and α, β- and γ-HCH concentrations (Figure 2). In contrast, findings from other studies indicate that adult males carry higher burdens of any of these chemicals than females [21,26,33,34]. According to Reijnders [35], a plateau in concentrations is reached at about 4 years because intake and excretion are balanced. Mature female marine mammals lose organochlorines during gestation and lactation [36,38], resulting in a reduction of the organochlorine burden. In contrast, males continue to accumulate organochlorines throughout life [37]. In the present study, most of the seals were young; especially the ringed seals from West Greenland and, therefore, no difference between the sexes could be expected.

environmental-analytical-toxicology-Level-pollutants

Figure 2: Level of pollutants in harbour and ringed seals separated by sex (ng/g lipid weight), N = number, HCH = hexachlorocyclohexane, PCB = polychlorinated biphenyls, DDT = dichlorodiphenyltrichlorethane, DDE = dichlorodiphenyldichlorethane.

Age correlation was insignificant (not shown), most likely due to the short age gradient of the investigated seals and the low representation of seals of higher age (Table 1). Young harbour seals already showed higher organochlorine concentrations when compared to ringed seals, most likely due to a transfer of the burden from contaminated female harbour seals during lactation [38]. In harbour seals from the Dutch Wadden Sea, newborns showed an even higher PCB burden than subadults [33,35]. Birnbaum [39] and Debier et al. [37] showed for harbour and grey seals that higher chlorinated PCB congeners are transferred in higher concentrations through the milk than lower chlorinated ones.

In summary the present study showed that female harbour seals infected with phocine distemper virus carried higher concentrations of organochlorine confirming previous investigations from other areas [24]. All organochlorines analysed in this investigation were found in seals from German and Greenlandic waters. HCH and HCB levels showed a significant decline but PCBs, DDT and DDE did not decrease significantly. Despite decreasing concentrations, PCBs and DDE burdens are still high (Table 4). Pathological findings such as loss of bone structure, leiomyoma and occlusion of the uterus associated with high organochlorine burdens for ringed and grey seals from the Baltic [11,12,14] were not found in harbour seals from the North Sea [7,19]. However, concentrations of those substances are still at levels known to affect the immune and endocrine systems and to cause vitamin A deficiency in harbour seals and porpoises from the North Sea [17,18,40-42]. Therefore, a contribution of organochlorines to the severity of mass mortalities and effects in seals with high burdens cannot be ruled out. Additionally, harbour seals from the Wadden Sea are also exposed to other pollutants such as perfluorooctane sulfonate (PFOS), polybrominated diphenyl ethers (PBDEs) and heavy metals [31,43-45] as well as other effects of anthropogenic activities [4] so that continuous pressure on the health of the animals needs to be assumed and further investigations should be carried out.

Acknowledgements

We acknowledge the German Federal Environmental Foundation for sponsoring the project. Harbour seals were collected in the course of investigations funded by the Ministry of Agriculture, Environment and Rural Development of Schleswig-Holstein and the Department “National Park and Marine Conservation” of the Schleswig-Holstein Agency for Coastal Defence, National Park and Marine Conservation. We thank people collecting animals and helping with sampling material. The sampling of ringed seals from Greenland was funded by the Danish Environmental Protection Agency as part of the environmental support programme Dancea. We are grateful to the hunters who secured the seal samples.

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