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Toxaphene in the aquatic environment of Greenland
Environmental Pollution 200 (2015) 140e148
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Toxaphene in the aquatic environment of Greenland t b, Rune Dietz b Katrin Vorkamp a, *, Frank F. Rige a b
Aarhus University, Department of Environmental Science, Arctic Research Centre, Frederiksborgvej 399, DK-4000 Roskilde, Denmark Aarhus University, Department of Bioscience, Arctic Research Centre, Frederiksborgvej 399, DK-4000 Roskilde, Denmark
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 November 2014 Received in revised form 4 February 2015 Accepted 5 February 2015 Available online 26 February 2015
The octa- and nonachlorinated bornanes (toxaphene) CHBs 26, 40, 41, 44, 50 and 62 were analysed in Arctic char (Salvelinus alpinus), shorthorn sculpin (Myoxocephalus scorpius), ringed seal (Pusa hispida) and black guillemot eggs (Cepphus grylle) from Greenland. Despite their high trophic level, ringed seals had the lowest concentrations of these species, with a S6Toxaphene median concentration of 13e20 ng/g lipid weight (lw), suggesting metabolisation. The congener composition also suggests transformation of nona- to octachlorinated congeners. Black guillemot eggs had the highest concentrations (S6Toxaphene median concentration of 971 ng/g lw). Although concentrations were higher in East than in West Greenland differences were smaller than for other persistent organic pollutants. In a circumpolar context, toxaphene had the highest concentrations in the Canadian Arctic. Time trend analyses showed significant decreases for black guillemot eggs and juvenile ringed seals, with annual rates of 5 to 7% for S6Toxaphene. The decreases were generally steepest for CHBs 40, 41 and 44. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Arctic char Bioaccumulation Black guillemot eggs Ringed seal Shorthorn sculpin Trends
1. Introduction Originally used as a trademark by the US manufacturer Hercules Incorporated, “toxaphene” is now generally used for complex insecticidal mixtures of polychlorobornanes and camphenes. Depending on the manufacturing process, products likely differ in chlorination degree and congener composition, leading to a theoretical number of ten thousands of congeners (Vetter, 1993). The former Soviet Union produced a similar product called polychloropinene in an estimated quantity of 160 000 tons (Trukhin et al., 2007). The US production peaked in 1975, at an annual production of at least 27 000 metric tons, registered for three manufacturers in 1975 (ATSDR, 2010). An accountable cumulative toxaphene usage of 450 000 tons was calculated in a global inventory, with an interpolated total usage from 1950 to 1993 of 1.33 million tons (Voldner and Li, 1993). This would place toxaphene in the same production volume category as polychlorinated biphenyls (PCBs), which had a cumulative production of 1.3 million tons (Breivik et al., 2002), and DDT, which was produced at 2.6 million tons (Voldner and Li, 1995). The highest usage of >100 000 tons of toxaphene was documented for the USA, while >10 000 tons were registered for the former Soviet Union, Germany, Brazil, Colombia, Egypt and possibly other countries * Corresponding author. E-mail address: [email protected] (K. Vorkamp). http://dx.doi.org/10.1016/j.envpol.2015.02.014 0269-7491/© 2015 Elsevier Ltd. All rights reserved.
(Voldner and Li, 1995). The use of toxaphene has also been reported for Sudan, Algeria and other African countries, causing runoff into the river Nile (de Geus et al., 1999; Voldner and Li, 1995). According to Voldner and Li (1995), >1000 tons were used in India and China and minor amounts in many other countries. Toxaphene was mainly used for pest control on cotton crops in the Southern United States, with minor applications (<15%) on other crops and livestock. A source in the Northern United States and Canada might have been the use in sport fishing to control fish stocks (ATSDR, 2010). Toxaphene is highly toxic to aquatic organisms, in particular marine fish (de Geus et al., 1999), and has been classified as possibly carcinogenic to humans by the International Agency for Research on Cancer (IARC, 2001). The USA banned toxaphene in 1982, however, according to ATSDR (2010), several US facilities still handled toxaphene in 2008. Toxaphene was among the initial 12 compounds listed by the Stockholm Convention on Persistent Organic Pollutants (POPs), which entered into force in 2004 and aims to achieve a global phase out of persistent, bioaccumulative and toxic compounds transported over long distances. The North American Great Lakes are probably the best studied region with regard to the environmental accumulation of toxaphene (e.g. Muir et al., 2004). Time trends have shown decreases of toxaphene in fish of the Great Lakes since the early 1980s, with a slightly lagged decrease in Lake Superior (e.g. Glassmeyer et al., 1997; Hickey et al., 2006). Despite its primary use in North
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America, toxaphene has also been detected in the European environment, including fish in the North Sea (de Boer and Wester, 1993) and sediment cores in a remote Scottish lake, showing a steep increase of toxaphene in the 1960s (Rose et al., 2001). Time trends extending to recent years, e.g. in eggs of tawny owl (Strix aluco) from Norway, showed a decrease of toxaphene from the 1980s (Bustnes et al., 2007). Toxaphene is also present in Arctic air and water (Bidleman et al., 1995) as well as fish and wildlife (Muir et al., 1988; Vorkamp et al., 2004a, 2008, 2014; Wolkers et al., 1998). Despite its significance as an insecticide and obvious ubiquitous distribution, information on toxaphene in the environment is sparse. This might be related to difficulties in analysing the complex mixture of congeners, which nowadays usually is based on specific individual standards (Braekevelt et al., 2001). This article presents results from ongoing studies in Greenland, including temporal trends in marine and freshwater species, circumpolar geographical trends and considerations on food web bioaccumulation and biomagnification. 2. Materials and methods 2.1. Sample collection The marine samples were obtained from local hunters at Qeqertarsuaq in Central West Greenland (69140 5000 N 53 320 0000 W) and Ittoqqortoormiit in Central East Greenland (70 290 0700 N 21580 0000 W) between 1986 and 2012. The samples of landlocked Arctic char originate from a lake near Isortoq in Southwest Greenland (61580 5000 N 47 300 1000 W). A map with the sampling locations is shown in the Supporting Information (Fig. S1). Shorthorn sculpin were caught by jigs and packed whole in polyethylene plastic bags for subsequent storage in a freezer. Only female sculpins were collected. The age of seals was determined according to Dietz et al. (1991). While only juvenile seals (4 years of age) were analysed from West Greenland, separate time trends were established for juvenile and adult seals in East Greenland. Detailed information on sample collection has been published previously t et al., 2010; Vorkamp et al., 2004b). An overview of the biota (Rige samples and their biological characteristics is given in Tables S1eS3 of the Supporting Information. 2.2. Chemical analysis The analytical method was described in detail by Vorkamp et al. (2004a) and has not been changed significantly. The analytical standards of the octa- and nonachlorinated bornanes CHBs 26, 40, 41, 44, 50 and 62 were originally purchased from LGC Standards (former Promochem, Wesel, Germany), but discontinued production required a change of manufacturer in 2012. For the quantification of the 2012 samples, CHBs 26, 50 and 62 were purchased from Cambridge Isotope Laboratories (CIL, Tewksbury, MA, USA), CHBs 40 and 41 were purchased from Wellington Laboratories (Guelph, Ont., Canada) and CHB 44 was purchased from Dr. Ehrenstorfer (Augsburg, Germany). Alternative nomenclatures of the target analytes are given in Table S4 of the Supporting Information. The samples were homogenised, dried with sodium sulphate or diatomaceous earth and spiked with PCB-198 (LGC Standards) for recovery determination. The compounds were Soxhlet extracted, using 350 ml of a mixture of n-hexane:acetone (4:1). The extracts were reduced in volume and cleaned up on a multilayer column packed bottom-to-top with 5 g aluminium oxide (10% water), 1 g activated silica (24 h at 160 C), 5 g activated silica (with sulphuric acid) and 1 cm anhydrous Na2SO4. The columns were eluted with 250 ml n-hexane, which subsequently was evaporated to <1 ml by
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rotary evaporation and under nitrogen. 13C-trans-chlordane (CIL) was added as a syringe standard for quantification, and the samples were adjusted with iso-octane to a precise volume of 1 ml. The extracts were analysed by gas chromatographyemass spectrometry (GCeMS) with electron capture negative ionisation (ECNI) on an Agilent GC HP6890 and MS HP5973. Methane was used as the ionisation gas at a pressure of 1.9 104 torr. The transfer line was at 280 C and the ion source temperature was kept at 150 C. The capillary column was a 60 m DB-5 (J&W Scientific; 0.25 mm inner diameter; 0.25 mm film thickness). The temperature programme was as follows: 90 C (1 min), increase to 220 C at a rate of 50 C min1, increase to 260 C at rate of 5 C min1, isotherm for 9.3 min, increase to 310 C at a rate of 50 C min1, 18.1 min at 310 C. The samples were processed in batches of 12e19 individual samples, 1e2 duplicate analyses, a procedural blank and 2 samples of an internal reference material (sand eel oil). Recovery correction was not performed as only samples with recoveries >80% were accepted. Blanks were below the limits of detection in all batches. Duplicates generally showed good agreement (Table S5 of the Supporting Information). Detection limits for each species are summarised in Table S6 of the Supporting Information. Although detection limits were higher in early than in more recent analyses, only few samples were below detection limits (Table S7 of the Supporting Information). Precision was monitored by plotting the concentrations of the internal reference material in control charts with warning and action limits (two and three times the standard deviation, respectively). The laboratory participated in the QUASIMEME proficiency testing scheme for toxaphene until it was discontinued in 2007. 2.3. Data analysis S6Toxaphene is the sum of the individual CHBs 26, 40, 41, 44, 50 and 62. Concentrations below detection limits were set to zero in calculations of S6Toxaphene. Prior to the statistical analyses, the concentrations were log-transformed to reduce skewness and thereby meet the assumption of normal distribution and homogenous variances. Analyses of variance (ANOVA) and Tukey's post hoc test were applied to test for differences between species and age groups. Linear mixed effect analyses (LME) with location as factor and sampling year as random (nested) factor were performed to test differences in log-mean concentrations between West and East Greenland in cases of shorthorn sculpin and juvenile ringed seals. The analyses of temporal trends followed the procedure used in temporal trend assessments of the International Council for the Exploration of the Sea (ICES). The method is a robust regressionbased analysis to detect temporal trends (Nicholson et al., 1998). The median concentration is used as yearly contaminant index value and was chosen instead of the mean concentration because it is less influenced by concentrations below detection limits and possible outliers. The total variation over time is divided into a linear and a non-linear component. Log-linear regression analysis was applied to describe the linear component and a three year running mean smoother was applied to describe the non-linear component. The linear and non-linear components were tested by means of an ANOVA. The statistical trend analyses were performed using the free software R version 2.15.2 (R Core Team, 2012). 3. Results and discussion 3.1. Bioaccumulation of toxaphene As sampling of shorthorn sculpin was discontinued in 2004, this is the last year with data for all sample types, as specified in
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Table 1 Median toxaphene concentrations (ng/g lipid weight) and lipid content of the most recent samples of this study. Juveniles: 4 years. Mean values and ranges are given in Table S7 of the Supporting Information. Sampling locations are shown in Fig. S1 of the Supporting Information. Species
Location
Year
Tissue
N
Lipid (%)
CHB 26
CHB 40
CHB 41
CHB 44
CHB 50
CHB 62
S6Toxaphene
Arctic char Shorthorn sculpin Shorthorn sculpin Ringed seals, juveniles Ringed seal, juveniles Ringed seals, adult Black guillemot
Isortoq West Greenland East Greenland West Greenland East Greenland East Greenland East Greenland
2012 2004 2004 2012 2012 2012 2012
Muscle Liver Liver Blubber Blubber Blubber Egg
15 20 20 15 14 6 10
0.5 12.8 10.5 93.2 92.9 93.1 10.1
27.5 12.0 49.2 2.62 3.45 4.15 144
3.28 3.09 8.76 0.29 0.36 0.49 69.6
2.62 3.56 11.1 0.72 0.97 1.22 24.9
8.73 3.55 13.6 0.83 0.98 1.16 26.2
65.1 15.9 68.1 2.15 3.22 3.70 238
13.0 4.34 30.1 0.78 1.48 1.81 70.1
122 41.0 183 6.64 9.51 11.5 563
Table S1 of the Supporting Information. For Arctic char, ringed seals and black guillemot, the most recent results are from 2012 (Table 1). Lipid-weight concentrations of S6Toxaphene in landlocked Arctic char and animals from East Greenland collected in 2004 increased in the order ringed seal (juvenile) ¼ ringed seal (adult) < Arctic char < shorthorn sculpin < black guillemot eggs (Tukey's multiple comparisons of mean, p < 0.05) (Fig. 1A). This order is different from that of e.g. PBDEs analysed in the same sample types, which placed lipid-normalised concentrations in ringed seals between those of the fish species and black guillemot eggs (Vorkamp et al., 2004a). Although ringed seals do not directly prey on the fish species of our study, their trophic level is higher than that of shorthorn sculpin or Arctic char. Based on wet weight, the concentrations increase in a slightly different order, i.e. Arctic char < ringed seals (juvenile) ¼ shorthorn sculpin ¼ ringed seal (adults) < black guillemot eggs (Tukey's multiple comparisons of mean, p < 0.05). The high concentrations in the black guillemot eggs support biomagnification of toxaphene, while the low concentrations in the ringed seals do not. Previous studies have indicated that toxaphene is less bioaccumulative than other organochlorine compounds (e.g. PCBs, chlordanes and p,p0 -DDE) in ringed seals (Routti et al., 2009; Wolkers et al., 1998). Biomagnification factors between Arctic cod or Arctic char and ringed seals were 0.1e0.2 in the Canadian Arctic (Hargrave et al., 1993), which is consistent with a concentration ratio of 0.1 for S6Toxaphene in ringed seals and Arctic char of our study. Similarly, toxaphene levels in polar cod liver were higher than in ringed seal blubber in a study from Svalbard (Føreid et al., 2000). Consequently, toxaphene concentrations in polar bear were below or at the same level as those in polar cod, while CB-153, for example, was about 30 times higher in polar bears than in polar cod (Føreid et al., 2000). Zhu and Norstrom (1993) likewise found that the bioaccumulation potential of toxaphene was only about 4% of that of PCBs. Furthermore, in contrast to PCBs, toxaphene concentrations were found not to increase with age of the ringed seals (Wolkers et al., 1998), which is confirmed by the absence of significant differences between juvenile and adult ringed seals from East Greenland in our study (ANOVA, p ¼ 0.08) (Fig. 1A). Fig. 1B shows the pattern of individual toxaphene congeners in the four sample types. The patterns of shorthorn sculpin and black guillemot are similar, except for relatively more CHB 40 and less CHB 26 in the black guillemot eggs. However, compared with the fish species and the black guillemot eggs, the ringed seals have a smaller percentage of the nonachlorinated congeners CHB 50 and CHB 62, while percentages of CHBs 40, 41 and 44 were higher. This pattern agrees with the toxaphene profile described for ringed seals in the Canadian Arctic (Gouteux et al., 2005). Other studies generally agree in identifying CHB 26 and CHB 50 as the most recalcitrant congeners, which probably react to a lower degree with metabolic enzymes as they do not possess unsubstituted carbon atoms at the lateral carbon ring (Routti et al., 2009). Routti et al. (2009) discussed that CHB 44, which has two
Fig. 1. S6Toxaphene results for East Greenland black guillemot eggs, ringed seal blubber and shorthorn sculpin liver as well as Arctic char muscle. A: Mean concentrations and standard deviations (in ng/g lipid weight) for samples from 2004. B: Mean composition of S6Toxaphene, averaged for all samples. AC: Arctic char. SSE: Shorthorn sculpin East Greenland. RSE: Ringed seal East Greenland. BGE: Black guillemot eggs East Greenland.
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higher proportion in eggs based on lipid-normalised concentrations suggests a disproportionally high transfer of these congeners to the eggs. This may be related the timing of lipid mobilisation in relation to toxaphene accumulation or to variations in lipid composition. However, only total lipid was determined in our study, which did not allow studying a potential influence of different lipid fractions on the maternal transfer of toxaphene congeners. 3.2. Spatial trends of toxaphene
Fig. 2. Spatial differences in S6Toxaphene concentrations (ng/g lipid weight, lw) between animals from Central West Greenland and Central East Greenland. A: Shorthorn sculpin liver. B: Ringed seal blubber. Three outliers were removed from figure B: Central East Greenland 2000: 200 ng/g lw; Central West Greenland 2000: 206 ng/g lw; Central West Greenland 2001: 329 ng/g lw. Corresponding figures of individual toxaphene congeners are given in the Supporting Information (Figs. S2 and S3).
unchlorinated carbon atoms at the lateral ring, was more susceptible to biotransformation via phase I enzyme reactions in ringed seals. However, compared with the other species of our study, CHB 44 (and CHB 41) seem to accumulate to a higher degree in ringed seals. This would be consistent with a degradation of CHB 50 and CHB 62, which can lead to the formation of CHBs 40, 41 and 44, as shown for Atlantic salmon (Salmo salar) (Berntssen et al., 2012). Concentration ratios between adult ringed seals and Arctic char are lowest for CHB 50 (0.06) and highest for CHB 41 (0.40), which would be in line with this degradation process. Previous studies showed that the toxaphene composition in black guillemot eggs was significantly different from that of black guillemot livers, in terms of higher percentages of CHB 50 and CHB 62 in the eggs (Vorkamp et al., 2004a). CHB 50 and CHB 62 have the highest KOW values of these six congeners (Fisk et al., 1999) indicating a strong partitioning into the lipid rich eggs. However, their
In case of juvenile ringed seals and shorthorn sculpin, data were available from West and East Greenland and the same year (Fig. 2). A linear mixed effect analyses (LME) with sampling year as random (nested) factor showed that for both shorthorn sculpin and juvenile ringed seals the concentrations of S6Toxaphene were significantly lower in West Greenland than in East Greenland (LME, p < 0.001 and p ¼ 0.016, respectively). Plots of individual congeners are given in Figs. S2 and S3 of the Supporting Information. For toxaphene in black guillemot eggs, a significant East > West difference had been shown previously (Vorkamp et al., 2004a). Higher concentrations in East Greenland than in West Greenland have been observed repeatedly, for both legacy POPs (with the exception of hexachlorocyclohexane, HCH), polybrominated diphenyl ethers (PBDEs) and perfluoroalkyl substances t et al., 2004, 2008, 2013; Vorkamp et al., 2008). (PFASs) (Rige However, the East > West difference was smaller for toxaphene than for other legacy POPs in a previous comparison including ringed seals and black guillemot eggs (Vorkamp et al., 2004a, 2008). This might be related to the primary use of toxaphene in the USA from where emissions can reach the west coast of Greenland. However, this influence is still smaller than the impact on the east coast of Greenland suggesting more complex transport processes or larger inputs from the Eurasian region than anticipated. Findings were similar for the main congeners of the PentaBDE formulation, t et al., 2006; which had also mainly been used in the USA (Rige Vorkamp et al., 2008). The East/West ratio differs between the species, in the order shorthorn sculpin > black guillemot eggs > ringed seals (Vorkamp et al., 2004a). Shorthorn sculpin feeds at a lower trophic level and is more sedentary than black guillemot and ringed seal. Thus, shorthorn sculpin might be more directly exposed to the toxaphene transported to the Arctic from lower latitudes than are black guillemots and ringed seals, whose exposure is a result of more complex uptake and transformation processes in the food chain. Table 1 summarises the most recent toxaphene results for all species of this study. In a circumpolar context, toxaphene concentrations in ringed seals seem to increase towards the Western Canadian Arctic (Fig. 3), which supports inputs of toxaphene to the Arctic from North America. S6Toxaphene concentrations in ringed seals from Nunavik in the Eastern Canadian Arctic were about 20 ng/g lw in 1999/2000, i.e. slightly higher than the results from Greenland (Gouteux et al., 2005). In Hudson Bay and Pangnirtung (Eastern Canadian Arctic), recent measurements showed S6Toxaphene concentrations at about 30 ng/g lw (Fig. 3). Toxaphene levels in ringed seals from the Russian Arctic were lower, i.e. 5e15 ng/g lw (Savinov et al., 2011). Ringed seals from Svalbard had toxaphene levels that also were 2e10 times lower than those of ringed seals from the Canadian Arctic (Wolkers et al., 1998). The authors emphasised that this trend was opposite to that of PCBs, which had 5 times higher concentrations in ringed seals from Svalbard. The concentrations of 30e50 ng/g lw reported by Wolkers et al. (1998) were in line with the earliest measurements in ringed seals from East Greenland. Somewhat lower concentrations of 6e10 ng/g lw were reported by
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Fig. 3. Spatial trend of SToxaphene in ringed seal blubber of the Arctic, based on arithmetic or geometric means. Data from Føreid et al. (2000) for female and male ringed seals from Svalbard collected in 1992 and aged 1e17 (mean 6) years (Sum of CHBs 26, 50 and 62), Gouteux et al. (2005) for male ringed seals from Nunavik, Canada collected in 1999/2000 and aged 9.2 ± 4.0 years (Sum of CHBs 26, 40, 41, 44, 50 and 62), Muir et al. (2013) and Muir (unpublished data) for female and juvenile male ringed seals from the remaining Canadian locations averaged for 2011 and 2012, except for results from Pangnirtung, which are from 2011 (Sum of CHBs 26, 40, 41, 44, 50 and 62) and Savinov et al. (2011) for female and male adult ringed seals from Russia collected in 2001 and 2002 (Sum of CHBs 26, 50 and 62). The data from Greenland are from 2012 (this study).
Føreid et al. (2000), for ringed seals presumably collected at about the same time as the samples in the study by Wolkers et al. (1998). In general, method differences might complicate comparisons between studies, however, the studies on ringed seals cited here all used congener-specific approaches. Toxaphene has often been found to be the predominant organochlorine group in landlocked Arctic char and other freshwater fish from the Canadian Arctic exceeding concentrations of other legacy POPs like PCBs and DDTs (Muir et al., 2013). SToxaphene concentrations in muscle of landlocked Arctic char of four Canadian lakes were approximately 3e80 ng/g ww during the period of 2003e2009 (Muir et al., 2013), whereas S6Toxaphene has been <1 ng/g ww in all sampling years of our study since 1999. Very few data are available on contaminant accumulation in shorthorn sculpin. Concentrations of S6Toxaphene between 180 and 222 ng/g lw were reported in a study of three locations in southern Greenland where shorthorn sculpin had been sampled in 2000 (Glasius et al., 2005). Interestingly, these concentrations are intermediate to ours from East and West Greenland (Fig. 2), based on data from 2002. Toxaphene was also widely detected in seabird eggs from Arctic Canada (Braune and Simon, 2004), but the studies did not include black guillemot eggs. The highest concentrations were found in eggs of black-legged kittiwake (64 ng/g ww) collected in 1993, which is lower than the earliest measurements of black guillemot eggs (111 ng/g ww) in 1999. Toxaphene levels were included in a study on black guillemot from Iceland covering the period 1976 to 1996 (Olafsdottir et al., 2005). Concentrations of CHB 26 in breast muscle of immature birds were approximately 0.5 ng/g ww.
Assuming a lipid content of 2.5% (Olafsdottir et al., 2001), this would be much lower than the earliest measurements of CHB 26 in black guillemot eggs (20 ng/g ww; 177 ng/g lw), even considering an accumulation of toxaphene with age and a disproportionally high transfer to the eggs as discussed above. In summary, all species show the East > West pattern frequently observed for other POPs, but possibly less pronounced for toxaphene. The concentrations in Greenland are lower than in the Canadian Arctic, which is different from patterns of other legacy POPs. Concentrations in the European and Russian Arctic seem to be similar to or lower than concentrations in Greenland. 3.3. Temporal trends All time trends have in common that they show decreasing concentrations of S6Toxaphene and individual congeners over time, with most decreases being statistically significant. Fig. 4 shows the time trend of S6Toxaphene for all sample types, and Table 2 summarises the trend statistics. Additional data and figures are available from the Supporting Information (Table S8; Figs. S4eS7). The overall decrease was expected, given the ban of toxaphene in the 1980s and the temporal development of other POPs banned t et al., 2010; in the same decade, for example that of PCBs (Rige Vorkamp et al., 2011; Dietz et al., 2013). The annual decrease of S6Toxaphene in adult ringed seals from East Greenland (4.5%) is comparable to that of S10-PCBs (3.4%), however, the study period is not identical (Vorkamp et al., 2011). Within the five sample types, the juvenile ringed seals from East Greenland showed the largest
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Fig. 4. Time trends of S6Toxaphene in Greenland. A: Arctic char (muscle). B: Juvenile ringed seals (blubber) from West Greenland. C: Juvenile ringed seals (blubber) from East Greenland. D: Adult ringed seals (blubber) from East Greenland. E: Black guillemot eggs. The filled dots are median values, the open circles are the individual values. The red line indicates a statistically significant trend. Blue stars are extreme values. Figures of individual toxaphene congeners are shown in the Supporting Information (Figs. S4eS7). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
annual change. Rather than biologically caused, this might be related to the longer time series dating back to 1986. Excluding the 1986 data point will still produce a significantly decreasing time trend for S6Toxaphene, however, the annual rate of decrease will be 6.5% instead of 7.2% (Table 2). As previously discussed for PCBs (Vorkamp et al., 2011), the main decrease might have taken place shortly after the ban in the 1980s and might not be caught by the time series starting around the year 2000. This could also be the reason for the non-significant decrease in the Arctic char time series, which started in 2004. From 1978 to 1988, toxaphene concentrations increased in walrus (Odobenus rosmarus rosmarus) from Greenland (Muir et al., 2000), which is consistent with the continued use of toxaphene until the late 1980s. A model of toxaphene accumulation in lake trout of the Great Lakes predicted the maximum concentration for the early 1980s, followed by a rapid and subsequently slowing decrease (Xia et al., 2011). The sediment core from Scotland indicated a peak for 1990 (Rose et al., 2001). These observations would be in line with maximum concentrations and the most rapid decline prior to our main monitoring period in Greenland starting around the year 2000. Regarding individual congeners, CHB 40 and CHB 41 were found to decrease significantly in Arctic char, at an annual rate of 17%
each (Table 2). As their contribution to S6Toxaphene is relatively small (Fig. 1B), this steeper decrease is not reflected in that of S6Toxaphene. In all sample types, CHB 40 and CHB 44 show the fastest decrease, while that of the most persistent congeners CHB 26 and CHB 50 was slowest. The time series for juvenile ringed seals from West Greenland and adult ringed seals from East Greenland cover the same time period and are very similar in the annual changes calculated for the individual congeners and S6Toxaphene (Table 2). They do not indicate major differences in the concentration developments at the west and east coast of Greenland although absolute levels are different (Fig. 2), probably a result of differences in air mass transport and thus, wildlife exposure as discussed above. A time trend for juvenile seals in West Greenland had been analysed previously (Vorkamp et al., 2008), covering the years 2000e2006. The extension to 2012 has sharpened the results for this time series: While the earlier trend of S6Toxaphene was nonsignificant, with an annual change of 4.3%, the updated trend is now statistically significant (p < 0.01) and gives an annual change t et al. (2010) analysed the statistical power of time of 5.2%. Rige series, in the context of their length, the number of samples per year, the random year to year variation, the significance level and the change to be detected. Within the Arctic Monitoring and
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Table 2 P-values for linear and non-linear trend components for Arctic char, juvenile ringed seals (4 years) from West Greenland as well as juvenile ringed seals (4 years), adult ringed seals and black guillemot eggs from East Greenland. F-values and residuals of the log-linear test are given in the Supporting Information. Congener
Time period
Log-linear trend component Annual change (%)
Non-linear trend component p-values
Arctic char (muscle)a CHB-26 2004e2012 0.8 0.84 CHB-40 2004e2012 17.1 <0.01 CHB-41 2004e2012 16.7 <0.01 CHB-44 2004e2012 11.5 0.16 CHB-50 2004e2012 3.7 0.54 CHB-62 2004e2012 10.0 0.52 2004e2012 4.9 0.38 S6Toxaphene Juvenile ringed seal (4 years) (blubber), Central West Greenland CHB-26 2000e2012 4.2 0.02 CHB-40 2000e2012 11.5 <0.01 CHB-41 2000e2012 8.0 <0.01 CHB-44 2001e2012 11.4 <0.01 CHB-50 2000e2012 6.7 <0.01 CHB-62b 2000e2012 e e S6Toxaphene 2000e2012 5.2 <0.01 Juvenile ringed seal (4 years) (blubber), Central East Greenland CHB-26 1986e2012 3.0 <0.01 CHB-40 1986e2012 10.9 <0.01 CHB-41 1986e2012 10.5 <0.01 CHB-44 2001e2012 10.4 <0.01 CHB-50 1986e2012 5.5 <0.01 CHB-62c 1986e2012 9.6 <0.01 S6Toxaphene 1986e2012 7.2 <0.01 Adult ringed seal (>4 years) (blubber), Central East Greenland CHB-26 2000e2012 4.3 0.06 CHB-40 2000e2012 11.7 <0.01 CHB-41 2000e2012 8.5 0.01 CHB-44 2001e2012 18.4 <0.01 CHB-50 2000e2012 5.6 0.01 CHB-62d 2000e2012 5.9 <0.01 S6Toxaphene 2000e2012 4.5 0.20 Black guillemot eggs, Central East Greenland CHB-26 1999e2012 2.1 0.32 CHB-40 1999e2012 7.1 <0.01 CHB-41 1999e2012 3.8 0.18 CHB-44 1999e2012 8.3 0.02 CHB-50 1999e2012 4.0 0.10 CHB-62 1999e2012 7.6 0.20 S6Toxaphene 1999e2012 4.7 0.03
p-values
e e e e e e e 0.07 0.17 0.09 0.02 0.12 e 0.12 0.04 1.0 1.0 0.04 0.02 0.24 0.19 0.14 0.15 0.15 0.28 0.18 0.02 0.68 0.62 1.0 0.46 0.63 0.57 0.38 1.0
a
The number of years did not allow test of the non-linear trend component. No time trend analysis possible because only data from 2006 and 2010 had a median above detection limits. c Data did not allow median calculations in 2001 and 2002. d Data did not allow median calculation in 2002. b
Assessment Programme (AMAP) only 8% of the time series had a statistical power of 80% to detect an annual change of 5% at a significance level of 5%. Based on these analyses, the authors concluded that more than 10 years of data were required before sufficient statistical power was obtained to detect significant cont et al., 2010). This agrees centration changes in the time series (Rige with the results of this study, which only showed significant trends for ringed seals and black guillemot eggs, i.e. the longest time series. Time trends in ringed seals were also studied at four locations in the Canadian Arctic, but none of the time series showed a significant trend (Muir et al., 2013). This is unexpected as these time series also date back to the 1980s, however, they generally include only few data points prior to 2005. Interestingly, increasing concentrations have been observed in the more recent measurements (Muir et al., 2013), dividing the overall time trend into two phases.
Other time trend studies from the Arctic have mainly focussed on freshwater fish. Lake trout (Salvelinus namaycush) and burbot (Lota lota) were studied in three lakes of the Yukon Territory, Canada from 1993 to 2003 (Ryan et al., 2005), however, with inconclusive results: Toxaphene decreased in lake trout muscle, but not in burbot liver for which a >200% increase was observed in Lake Quiet. An update focussing on Lake Laberge did show significantly decreasing concentrations of toxaphene in lake trout, burbot and several other freshwater species. However, growth dilution and changes in ecosystem structures might have affected the organochlorine concentrations (Ryan et al., 2013). Updates from 2011 confirmed decreasing concentrations of toxaphene in lake trout from Lake Laberge, while no new data were available for burbot (Muir et al., 2013). Besides the Yukon lakes, temporal trends of toxaphene in the freshwater environment of the Canadian Arctic were studied for lake trout and burbot from the Great Slave Lake, sea-run Arctic char at two locations, burbot in the Mackenzie River and landlocked Arctic char in four lakes of the high Arctic (Muir et al., 2013). In agreement with observations for ringed seals, some of these time series showed recent or temporary increases of toxaphene, for example, toxaphene in burbot from the Mackenzie River was found to increase from 2001 to 2009, and then returned to the 2001 level. An upward trend was also observed in landlocked Arctic char between 2003 and 2010, which the authors attributed to mobilisation of old sources in the area. However, the trends including samples from the 1990s generally showed lower concentrations in recent measurements. Peregrine falcon eggs (Falco peregrinus) collected in Greenland between 1986 and 2003 did not show any significant trends for S6Toxaphene or individual congeners (Vorkamp et al., 2014). Using the same approach as in this study, four congeners showed a nonsignificant positive trend, while only CHB 26, CHB 40 and S6Toxaphene showed a decreasing, but non-significant trend. These results were different from those of chlordane-related pesticides in the same samples, a compound group with a similar phase out history, but lower production volumes than toxaphene. The authors discussed that secondary sources of toxaphene in combination with a long life span of the peregrine falcons might have caused their exposure. Outside the Arctic, overall decreases of toxaphene were found for fish of the Great Lakes, for which toxaphene concentrations were monitored from 1989 to 2009 (Chernyak et al., 2005; Glassmeyer et al., 1997; Hickey et al., 2006; Xia et al., 2012). Decreases of toxaphene were also observed in beluga (Delphinapterus leucas) from the St. Lawrence River in Canada, during the period 1988e1999 (Gouteux et al., 2003). The authors remarked that the decrease by approximately a factor of 2 was comparable to the emission reductions in the Southern United States. In Europe, toxaphene levels in eggs of tawny owl from Norway decreased by a factor of 4 from the first study period (1986e1995) to the second one (1998e2004), while no trend was found in black guillemot muscle collected in Iceland between 1977 and 1992 (Olafsdottir et al., 2005). In summary, there is evidence of decreasing concentrations of toxaphene in most species and study areas although species from the marine environment have been studied to a lesser extent. Few exceptions from the overall decreases exist, which might be related to the time period covered by the time trend study and thus the power of the time series. Furthermore, ecological factors, such as varying feeding behaviour, might play a role in these observations, as well as exposure to newly released toxaphene from secondary sources.
K. Vorkamp et al. / Environmental Pollution 200 (2015) 140e148
4. Conclusions Toxaphene accumulates strongly in black guillemot eggs, but seems to undergo transformation in ringed seals, with consequences of a lower exposure to polar bears compared with other POPs. Although toxaphene follows the East Greenland > West Greenland pattern observed for other POPs, its circumpolar trend is different. Highest concentrations occur in the North American Arctic, probably a result of the main use of toxaphene in the USA. Toxaphene concentrations have been decreasing in Arctic char, black guillemot eggs and ringed seals from Greenland, which supports time trend studies of other species and in other regions. Observations in the Canadian Arctic of recent toxaphene increases are not apparent in the Greenland time series as of 2012. Acknowledgements The study was funded by the Danish Cooperation for Environment in the Arctic (DANCEA) of the Danish Environmental Protection Agency. The authors wish to thank Derek Muir for help with Fig. 3 and Sigga Joensen, Annegrete Ljungqvist and Birgit Groth for technical assistance in the laboratory. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2015.02.014. References ATSDR, 2010. Draft Toxicological Profile for Toxaphene. U.S. Department of Health and Human Services. Public Health Service. Agency for Toxic Substances and Disease Registry. Berntssen, M.H.G., Lundebye, A.-K., Hop-Johannessen, L., Lock, E.-J., 2012. Dechlorination of the dietary nona-chlorinated toxaphene congeners 62 and 50 into the octa-chlorinated toxaphene congeners 44 and 40 in zebrafish (Danio rerio) and Atlantic salmon (Salmo salar). Aquat. Toxicol. 112e113, 54e61. Bidleman, T.F., Falconer, R.L., Wallab, M.D., 1995. Toxaphene and other organochlorine compounds in air and water at Resolute Bay, N.W.T., Canada. Sci. Total Environ. 160/161, 55e63. Braekevelt, E., Tomy, G.T., Stern, G.A., 2001. Comparison of an individual congener standard and a technical mixture for the quantification of toxaphene in environmental matrices by HRGC/ECNI-HRMS. Environ. Sci. Technol. 35, 3513e3518. Braune, B.M., Simon, M., 2004. Trace elements and halogenated organic compounds in Canadian Arctic seabirds. Mar. Poll. Bull. 48, 986e1008. Breivik, K., Sweetman, A., Pacyna, J.M., Jones, K.C., 2002. Towards a global historical emission inventory for selected PCB congeners e a mass balance approach: 1. Global production and consumption. Sci. Total Environ. 290 (1e3), 181e198. Bustnes, J.O., Yoggoz, N.G., Bangjord, G., Polder, A., Skaare, J.E., 2007. Temporal trends (1986-2004) of organochlorines and brominated flame retardants in tawny owl eggs from Northern Europe. Environ. Sci. Technol. 41, 8491e8497. Chernyak, S.M., Rice, C.P., Quintal, R.T., Begnoche, L.J., Hickey, J.P., Vinyards, B.T., 2005. Time trends (1983-1999) for organochlorines and polybrominated diphenyl ethers in rainbow smelt (Osmerus mordax) from Lakes Michigan, Huran, and Superior, USA. Environ. Toxicol. Chem. 24 (7), 1632e1641. de Boer, J., Wester, P.G., 1993. Determination of toxaphene in human milk from Nicaragua and in fish and marine mammals from the Northeastern Atlantic and the North Sea. Chemosphere 27 (10), 1879e1890. de Geus, H.-J., Besselink, H., Brouwer, A., Klungsøyr, J., McHugh, B., Nixon, E., Rimkus, G.G., Wester, P.G., de Boer, J., 1999. Environmental occurrence, analysis, and toxicology of toxaphene compounds. Environ. Health Persp. 107 (Suppl. 1), 115e144. Dietz, R., Heide-Jørgensen, M.-P., Harkonen, T., Teilmann, J., Valentin, N., 1991. Age determination in European harbour seals Phoca vitulina L. Sarsia 76 (1e2), 17e21. t, F.F., Sonne, C., Born, E.W., Bechshøft, T., McKinney, M.A., Letcher, R.J., Dietz, R., Rige 2013. Three decades (1983e2010) of contaminant trends in East Greenland polar bears (Ursus maritimus). Part 1: legacy organochlorine contaminants. Environ. Int. 59, 485e493. Fisk, A.T., Rosenberg, B., Cymbalisty, C.D., Stern, G.A., Muir, D.C.G., 1999. Octanol/ water partition coefficients of toxaphene congeners determined by the “slowstirring” method. Chemosphere 39 (14), 2549e2562. Føreid, S., Rundberget, T., Severinsen, T., Wiig, Ø., Skaare, J.U., 2000. Determination of toxaphenes in fish and marine mammals. Chemosphere 41, 521e528. Glasius, M., Christensen, J.H., Platz, J., Vorkamp, K., 2005. Halogenated organic
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Toxaphene in the aquatic environment of Greenland t b, Rune Dietz b Katrin Vorkamp a, *, Frank F. Rige a b
Aarhus University, Department of Environmental Science, Arctic Research Centre, Frederiksborgvej 399, DK-4000 Roskilde, Denmark Aarhus University, Department of Bioscience, Arctic Research Centre, Frederiksborgvej 399, DK-4000 Roskilde, Denmark
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 November 2014 Received in revised form 4 February 2015 Accepted 5 February 2015 Available online 26 February 2015
The octa- and nonachlorinated bornanes (toxaphene) CHBs 26, 40, 41, 44, 50 and 62 were analysed in Arctic char (Salvelinus alpinus), shorthorn sculpin (Myoxocephalus scorpius), ringed seal (Pusa hispida) and black guillemot eggs (Cepphus grylle) from Greenland. Despite their high trophic level, ringed seals had the lowest concentrations of these species, with a S6Toxaphene median concentration of 13e20 ng/g lipid weight (lw), suggesting metabolisation. The congener composition also suggests transformation of nona- to octachlorinated congeners. Black guillemot eggs had the highest concentrations (S6Toxaphene median concentration of 971 ng/g lw). Although concentrations were higher in East than in West Greenland differences were smaller than for other persistent organic pollutants. In a circumpolar context, toxaphene had the highest concentrations in the Canadian Arctic. Time trend analyses showed significant decreases for black guillemot eggs and juvenile ringed seals, with annual rates of 5 to 7% for S6Toxaphene. The decreases were generally steepest for CHBs 40, 41 and 44. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Arctic char Bioaccumulation Black guillemot eggs Ringed seal Shorthorn sculpin Trends
1. Introduction Originally used as a trademark by the US manufacturer Hercules Incorporated, “toxaphene” is now generally used for complex insecticidal mixtures of polychlorobornanes and camphenes. Depending on the manufacturing process, products likely differ in chlorination degree and congener composition, leading to a theoretical number of ten thousands of congeners (Vetter, 1993). The former Soviet Union produced a similar product called polychloropinene in an estimated quantity of 160 000 tons (Trukhin et al., 2007). The US production peaked in 1975, at an annual production of at least 27 000 metric tons, registered for three manufacturers in 1975 (ATSDR, 2010). An accountable cumulative toxaphene usage of 450 000 tons was calculated in a global inventory, with an interpolated total usage from 1950 to 1993 of 1.33 million tons (Voldner and Li, 1993). This would place toxaphene in the same production volume category as polychlorinated biphenyls (PCBs), which had a cumulative production of 1.3 million tons (Breivik et al., 2002), and DDT, which was produced at 2.6 million tons (Voldner and Li, 1995). The highest usage of >100 000 tons of toxaphene was documented for the USA, while >10 000 tons were registered for the former Soviet Union, Germany, Brazil, Colombia, Egypt and possibly other countries * Corresponding author. E-mail address: [email protected] (K. Vorkamp). http://dx.doi.org/10.1016/j.envpol.2015.02.014 0269-7491/© 2015 Elsevier Ltd. All rights reserved.
(Voldner and Li, 1995). The use of toxaphene has also been reported for Sudan, Algeria and other African countries, causing runoff into the river Nile (de Geus et al., 1999; Voldner and Li, 1995). According to Voldner and Li (1995), >1000 tons were used in India and China and minor amounts in many other countries. Toxaphene was mainly used for pest control on cotton crops in the Southern United States, with minor applications (<15%) on other crops and livestock. A source in the Northern United States and Canada might have been the use in sport fishing to control fish stocks (ATSDR, 2010). Toxaphene is highly toxic to aquatic organisms, in particular marine fish (de Geus et al., 1999), and has been classified as possibly carcinogenic to humans by the International Agency for Research on Cancer (IARC, 2001). The USA banned toxaphene in 1982, however, according to ATSDR (2010), several US facilities still handled toxaphene in 2008. Toxaphene was among the initial 12 compounds listed by the Stockholm Convention on Persistent Organic Pollutants (POPs), which entered into force in 2004 and aims to achieve a global phase out of persistent, bioaccumulative and toxic compounds transported over long distances. The North American Great Lakes are probably the best studied region with regard to the environmental accumulation of toxaphene (e.g. Muir et al., 2004). Time trends have shown decreases of toxaphene in fish of the Great Lakes since the early 1980s, with a slightly lagged decrease in Lake Superior (e.g. Glassmeyer et al., 1997; Hickey et al., 2006). Despite its primary use in North
K. Vorkamp et al. / Environmental Pollution 200 (2015) 140e148
America, toxaphene has also been detected in the European environment, including fish in the North Sea (de Boer and Wester, 1993) and sediment cores in a remote Scottish lake, showing a steep increase of toxaphene in the 1960s (Rose et al., 2001). Time trends extending to recent years, e.g. in eggs of tawny owl (Strix aluco) from Norway, showed a decrease of toxaphene from the 1980s (Bustnes et al., 2007). Toxaphene is also present in Arctic air and water (Bidleman et al., 1995) as well as fish and wildlife (Muir et al., 1988; Vorkamp et al., 2004a, 2008, 2014; Wolkers et al., 1998). Despite its significance as an insecticide and obvious ubiquitous distribution, information on toxaphene in the environment is sparse. This might be related to difficulties in analysing the complex mixture of congeners, which nowadays usually is based on specific individual standards (Braekevelt et al., 2001). This article presents results from ongoing studies in Greenland, including temporal trends in marine and freshwater species, circumpolar geographical trends and considerations on food web bioaccumulation and biomagnification. 2. Materials and methods 2.1. Sample collection The marine samples were obtained from local hunters at Qeqertarsuaq in Central West Greenland (69140 5000 N 53 320 0000 W) and Ittoqqortoormiit in Central East Greenland (70 290 0700 N 21580 0000 W) between 1986 and 2012. The samples of landlocked Arctic char originate from a lake near Isortoq in Southwest Greenland (61580 5000 N 47 300 1000 W). A map with the sampling locations is shown in the Supporting Information (Fig. S1). Shorthorn sculpin were caught by jigs and packed whole in polyethylene plastic bags for subsequent storage in a freezer. Only female sculpins were collected. The age of seals was determined according to Dietz et al. (1991). While only juvenile seals (4 years of age) were analysed from West Greenland, separate time trends were established for juvenile and adult seals in East Greenland. Detailed information on sample collection has been published previously t et al., 2010; Vorkamp et al., 2004b). An overview of the biota (Rige samples and their biological characteristics is given in Tables S1eS3 of the Supporting Information. 2.2. Chemical analysis The analytical method was described in detail by Vorkamp et al. (2004a) and has not been changed significantly. The analytical standards of the octa- and nonachlorinated bornanes CHBs 26, 40, 41, 44, 50 and 62 were originally purchased from LGC Standards (former Promochem, Wesel, Germany), but discontinued production required a change of manufacturer in 2012. For the quantification of the 2012 samples, CHBs 26, 50 and 62 were purchased from Cambridge Isotope Laboratories (CIL, Tewksbury, MA, USA), CHBs 40 and 41 were purchased from Wellington Laboratories (Guelph, Ont., Canada) and CHB 44 was purchased from Dr. Ehrenstorfer (Augsburg, Germany). Alternative nomenclatures of the target analytes are given in Table S4 of the Supporting Information. The samples were homogenised, dried with sodium sulphate or diatomaceous earth and spiked with PCB-198 (LGC Standards) for recovery determination. The compounds were Soxhlet extracted, using 350 ml of a mixture of n-hexane:acetone (4:1). The extracts were reduced in volume and cleaned up on a multilayer column packed bottom-to-top with 5 g aluminium oxide (10% water), 1 g activated silica (24 h at 160 C), 5 g activated silica (with sulphuric acid) and 1 cm anhydrous Na2SO4. The columns were eluted with 250 ml n-hexane, which subsequently was evaporated to <1 ml by
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rotary evaporation and under nitrogen. 13C-trans-chlordane (CIL) was added as a syringe standard for quantification, and the samples were adjusted with iso-octane to a precise volume of 1 ml. The extracts were analysed by gas chromatographyemass spectrometry (GCeMS) with electron capture negative ionisation (ECNI) on an Agilent GC HP6890 and MS HP5973. Methane was used as the ionisation gas at a pressure of 1.9 104 torr. The transfer line was at 280 C and the ion source temperature was kept at 150 C. The capillary column was a 60 m DB-5 (J&W Scientific; 0.25 mm inner diameter; 0.25 mm film thickness). The temperature programme was as follows: 90 C (1 min), increase to 220 C at a rate of 50 C min1, increase to 260 C at rate of 5 C min1, isotherm for 9.3 min, increase to 310 C at a rate of 50 C min1, 18.1 min at 310 C. The samples were processed in batches of 12e19 individual samples, 1e2 duplicate analyses, a procedural blank and 2 samples of an internal reference material (sand eel oil). Recovery correction was not performed as only samples with recoveries >80% were accepted. Blanks were below the limits of detection in all batches. Duplicates generally showed good agreement (Table S5 of the Supporting Information). Detection limits for each species are summarised in Table S6 of the Supporting Information. Although detection limits were higher in early than in more recent analyses, only few samples were below detection limits (Table S7 of the Supporting Information). Precision was monitored by plotting the concentrations of the internal reference material in control charts with warning and action limits (two and three times the standard deviation, respectively). The laboratory participated in the QUASIMEME proficiency testing scheme for toxaphene until it was discontinued in 2007. 2.3. Data analysis S6Toxaphene is the sum of the individual CHBs 26, 40, 41, 44, 50 and 62. Concentrations below detection limits were set to zero in calculations of S6Toxaphene. Prior to the statistical analyses, the concentrations were log-transformed to reduce skewness and thereby meet the assumption of normal distribution and homogenous variances. Analyses of variance (ANOVA) and Tukey's post hoc test were applied to test for differences between species and age groups. Linear mixed effect analyses (LME) with location as factor and sampling year as random (nested) factor were performed to test differences in log-mean concentrations between West and East Greenland in cases of shorthorn sculpin and juvenile ringed seals. The analyses of temporal trends followed the procedure used in temporal trend assessments of the International Council for the Exploration of the Sea (ICES). The method is a robust regressionbased analysis to detect temporal trends (Nicholson et al., 1998). The median concentration is used as yearly contaminant index value and was chosen instead of the mean concentration because it is less influenced by concentrations below detection limits and possible outliers. The total variation over time is divided into a linear and a non-linear component. Log-linear regression analysis was applied to describe the linear component and a three year running mean smoother was applied to describe the non-linear component. The linear and non-linear components were tested by means of an ANOVA. The statistical trend analyses were performed using the free software R version 2.15.2 (R Core Team, 2012). 3. Results and discussion 3.1. Bioaccumulation of toxaphene As sampling of shorthorn sculpin was discontinued in 2004, this is the last year with data for all sample types, as specified in
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Table 1 Median toxaphene concentrations (ng/g lipid weight) and lipid content of the most recent samples of this study. Juveniles: 4 years. Mean values and ranges are given in Table S7 of the Supporting Information. Sampling locations are shown in Fig. S1 of the Supporting Information. Species
Location
Year
Tissue
N
Lipid (%)
CHB 26
CHB 40
CHB 41
CHB 44
CHB 50
CHB 62
S6Toxaphene
Arctic char Shorthorn sculpin Shorthorn sculpin Ringed seals, juveniles Ringed seal, juveniles Ringed seals, adult Black guillemot
Isortoq West Greenland East Greenland West Greenland East Greenland East Greenland East Greenland
2012 2004 2004 2012 2012 2012 2012
Muscle Liver Liver Blubber Blubber Blubber Egg
15 20 20 15 14 6 10
0.5 12.8 10.5 93.2 92.9 93.1 10.1
27.5 12.0 49.2 2.62 3.45 4.15 144
3.28 3.09 8.76 0.29 0.36 0.49 69.6
2.62 3.56 11.1 0.72 0.97 1.22 24.9
8.73 3.55 13.6 0.83 0.98 1.16 26.2
65.1 15.9 68.1 2.15 3.22 3.70 238
13.0 4.34 30.1 0.78 1.48 1.81 70.1
122 41.0 183 6.64 9.51 11.5 563
Table S1 of the Supporting Information. For Arctic char, ringed seals and black guillemot, the most recent results are from 2012 (Table 1). Lipid-weight concentrations of S6Toxaphene in landlocked Arctic char and animals from East Greenland collected in 2004 increased in the order ringed seal (juvenile) ¼ ringed seal (adult) < Arctic char < shorthorn sculpin < black guillemot eggs (Tukey's multiple comparisons of mean, p < 0.05) (Fig. 1A). This order is different from that of e.g. PBDEs analysed in the same sample types, which placed lipid-normalised concentrations in ringed seals between those of the fish species and black guillemot eggs (Vorkamp et al., 2004a). Although ringed seals do not directly prey on the fish species of our study, their trophic level is higher than that of shorthorn sculpin or Arctic char. Based on wet weight, the concentrations increase in a slightly different order, i.e. Arctic char < ringed seals (juvenile) ¼ shorthorn sculpin ¼ ringed seal (adults) < black guillemot eggs (Tukey's multiple comparisons of mean, p < 0.05). The high concentrations in the black guillemot eggs support biomagnification of toxaphene, while the low concentrations in the ringed seals do not. Previous studies have indicated that toxaphene is less bioaccumulative than other organochlorine compounds (e.g. PCBs, chlordanes and p,p0 -DDE) in ringed seals (Routti et al., 2009; Wolkers et al., 1998). Biomagnification factors between Arctic cod or Arctic char and ringed seals were 0.1e0.2 in the Canadian Arctic (Hargrave et al., 1993), which is consistent with a concentration ratio of 0.1 for S6Toxaphene in ringed seals and Arctic char of our study. Similarly, toxaphene levels in polar cod liver were higher than in ringed seal blubber in a study from Svalbard (Føreid et al., 2000). Consequently, toxaphene concentrations in polar bear were below or at the same level as those in polar cod, while CB-153, for example, was about 30 times higher in polar bears than in polar cod (Føreid et al., 2000). Zhu and Norstrom (1993) likewise found that the bioaccumulation potential of toxaphene was only about 4% of that of PCBs. Furthermore, in contrast to PCBs, toxaphene concentrations were found not to increase with age of the ringed seals (Wolkers et al., 1998), which is confirmed by the absence of significant differences between juvenile and adult ringed seals from East Greenland in our study (ANOVA, p ¼ 0.08) (Fig. 1A). Fig. 1B shows the pattern of individual toxaphene congeners in the four sample types. The patterns of shorthorn sculpin and black guillemot are similar, except for relatively more CHB 40 and less CHB 26 in the black guillemot eggs. However, compared with the fish species and the black guillemot eggs, the ringed seals have a smaller percentage of the nonachlorinated congeners CHB 50 and CHB 62, while percentages of CHBs 40, 41 and 44 were higher. This pattern agrees with the toxaphene profile described for ringed seals in the Canadian Arctic (Gouteux et al., 2005). Other studies generally agree in identifying CHB 26 and CHB 50 as the most recalcitrant congeners, which probably react to a lower degree with metabolic enzymes as they do not possess unsubstituted carbon atoms at the lateral carbon ring (Routti et al., 2009). Routti et al. (2009) discussed that CHB 44, which has two
Fig. 1. S6Toxaphene results for East Greenland black guillemot eggs, ringed seal blubber and shorthorn sculpin liver as well as Arctic char muscle. A: Mean concentrations and standard deviations (in ng/g lipid weight) for samples from 2004. B: Mean composition of S6Toxaphene, averaged for all samples. AC: Arctic char. SSE: Shorthorn sculpin East Greenland. RSE: Ringed seal East Greenland. BGE: Black guillemot eggs East Greenland.
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higher proportion in eggs based on lipid-normalised concentrations suggests a disproportionally high transfer of these congeners to the eggs. This may be related the timing of lipid mobilisation in relation to toxaphene accumulation or to variations in lipid composition. However, only total lipid was determined in our study, which did not allow studying a potential influence of different lipid fractions on the maternal transfer of toxaphene congeners. 3.2. Spatial trends of toxaphene
Fig. 2. Spatial differences in S6Toxaphene concentrations (ng/g lipid weight, lw) between animals from Central West Greenland and Central East Greenland. A: Shorthorn sculpin liver. B: Ringed seal blubber. Three outliers were removed from figure B: Central East Greenland 2000: 200 ng/g lw; Central West Greenland 2000: 206 ng/g lw; Central West Greenland 2001: 329 ng/g lw. Corresponding figures of individual toxaphene congeners are given in the Supporting Information (Figs. S2 and S3).
unchlorinated carbon atoms at the lateral ring, was more susceptible to biotransformation via phase I enzyme reactions in ringed seals. However, compared with the other species of our study, CHB 44 (and CHB 41) seem to accumulate to a higher degree in ringed seals. This would be consistent with a degradation of CHB 50 and CHB 62, which can lead to the formation of CHBs 40, 41 and 44, as shown for Atlantic salmon (Salmo salar) (Berntssen et al., 2012). Concentration ratios between adult ringed seals and Arctic char are lowest for CHB 50 (0.06) and highest for CHB 41 (0.40), which would be in line with this degradation process. Previous studies showed that the toxaphene composition in black guillemot eggs was significantly different from that of black guillemot livers, in terms of higher percentages of CHB 50 and CHB 62 in the eggs (Vorkamp et al., 2004a). CHB 50 and CHB 62 have the highest KOW values of these six congeners (Fisk et al., 1999) indicating a strong partitioning into the lipid rich eggs. However, their
In case of juvenile ringed seals and shorthorn sculpin, data were available from West and East Greenland and the same year (Fig. 2). A linear mixed effect analyses (LME) with sampling year as random (nested) factor showed that for both shorthorn sculpin and juvenile ringed seals the concentrations of S6Toxaphene were significantly lower in West Greenland than in East Greenland (LME, p < 0.001 and p ¼ 0.016, respectively). Plots of individual congeners are given in Figs. S2 and S3 of the Supporting Information. For toxaphene in black guillemot eggs, a significant East > West difference had been shown previously (Vorkamp et al., 2004a). Higher concentrations in East Greenland than in West Greenland have been observed repeatedly, for both legacy POPs (with the exception of hexachlorocyclohexane, HCH), polybrominated diphenyl ethers (PBDEs) and perfluoroalkyl substances t et al., 2004, 2008, 2013; Vorkamp et al., 2008). (PFASs) (Rige However, the East > West difference was smaller for toxaphene than for other legacy POPs in a previous comparison including ringed seals and black guillemot eggs (Vorkamp et al., 2004a, 2008). This might be related to the primary use of toxaphene in the USA from where emissions can reach the west coast of Greenland. However, this influence is still smaller than the impact on the east coast of Greenland suggesting more complex transport processes or larger inputs from the Eurasian region than anticipated. Findings were similar for the main congeners of the PentaBDE formulation, t et al., 2006; which had also mainly been used in the USA (Rige Vorkamp et al., 2008). The East/West ratio differs between the species, in the order shorthorn sculpin > black guillemot eggs > ringed seals (Vorkamp et al., 2004a). Shorthorn sculpin feeds at a lower trophic level and is more sedentary than black guillemot and ringed seal. Thus, shorthorn sculpin might be more directly exposed to the toxaphene transported to the Arctic from lower latitudes than are black guillemots and ringed seals, whose exposure is a result of more complex uptake and transformation processes in the food chain. Table 1 summarises the most recent toxaphene results for all species of this study. In a circumpolar context, toxaphene concentrations in ringed seals seem to increase towards the Western Canadian Arctic (Fig. 3), which supports inputs of toxaphene to the Arctic from North America. S6Toxaphene concentrations in ringed seals from Nunavik in the Eastern Canadian Arctic were about 20 ng/g lw in 1999/2000, i.e. slightly higher than the results from Greenland (Gouteux et al., 2005). In Hudson Bay and Pangnirtung (Eastern Canadian Arctic), recent measurements showed S6Toxaphene concentrations at about 30 ng/g lw (Fig. 3). Toxaphene levels in ringed seals from the Russian Arctic were lower, i.e. 5e15 ng/g lw (Savinov et al., 2011). Ringed seals from Svalbard had toxaphene levels that also were 2e10 times lower than those of ringed seals from the Canadian Arctic (Wolkers et al., 1998). The authors emphasised that this trend was opposite to that of PCBs, which had 5 times higher concentrations in ringed seals from Svalbard. The concentrations of 30e50 ng/g lw reported by Wolkers et al. (1998) were in line with the earliest measurements in ringed seals from East Greenland. Somewhat lower concentrations of 6e10 ng/g lw were reported by
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Fig. 3. Spatial trend of SToxaphene in ringed seal blubber of the Arctic, based on arithmetic or geometric means. Data from Føreid et al. (2000) for female and male ringed seals from Svalbard collected in 1992 and aged 1e17 (mean 6) years (Sum of CHBs 26, 50 and 62), Gouteux et al. (2005) for male ringed seals from Nunavik, Canada collected in 1999/2000 and aged 9.2 ± 4.0 years (Sum of CHBs 26, 40, 41, 44, 50 and 62), Muir et al. (2013) and Muir (unpublished data) for female and juvenile male ringed seals from the remaining Canadian locations averaged for 2011 and 2012, except for results from Pangnirtung, which are from 2011 (Sum of CHBs 26, 40, 41, 44, 50 and 62) and Savinov et al. (2011) for female and male adult ringed seals from Russia collected in 2001 and 2002 (Sum of CHBs 26, 50 and 62). The data from Greenland are from 2012 (this study).
Føreid et al. (2000), for ringed seals presumably collected at about the same time as the samples in the study by Wolkers et al. (1998). In general, method differences might complicate comparisons between studies, however, the studies on ringed seals cited here all used congener-specific approaches. Toxaphene has often been found to be the predominant organochlorine group in landlocked Arctic char and other freshwater fish from the Canadian Arctic exceeding concentrations of other legacy POPs like PCBs and DDTs (Muir et al., 2013). SToxaphene concentrations in muscle of landlocked Arctic char of four Canadian lakes were approximately 3e80 ng/g ww during the period of 2003e2009 (Muir et al., 2013), whereas S6Toxaphene has been <1 ng/g ww in all sampling years of our study since 1999. Very few data are available on contaminant accumulation in shorthorn sculpin. Concentrations of S6Toxaphene between 180 and 222 ng/g lw were reported in a study of three locations in southern Greenland where shorthorn sculpin had been sampled in 2000 (Glasius et al., 2005). Interestingly, these concentrations are intermediate to ours from East and West Greenland (Fig. 2), based on data from 2002. Toxaphene was also widely detected in seabird eggs from Arctic Canada (Braune and Simon, 2004), but the studies did not include black guillemot eggs. The highest concentrations were found in eggs of black-legged kittiwake (64 ng/g ww) collected in 1993, which is lower than the earliest measurements of black guillemot eggs (111 ng/g ww) in 1999. Toxaphene levels were included in a study on black guillemot from Iceland covering the period 1976 to 1996 (Olafsdottir et al., 2005). Concentrations of CHB 26 in breast muscle of immature birds were approximately 0.5 ng/g ww.
Assuming a lipid content of 2.5% (Olafsdottir et al., 2001), this would be much lower than the earliest measurements of CHB 26 in black guillemot eggs (20 ng/g ww; 177 ng/g lw), even considering an accumulation of toxaphene with age and a disproportionally high transfer to the eggs as discussed above. In summary, all species show the East > West pattern frequently observed for other POPs, but possibly less pronounced for toxaphene. The concentrations in Greenland are lower than in the Canadian Arctic, which is different from patterns of other legacy POPs. Concentrations in the European and Russian Arctic seem to be similar to or lower than concentrations in Greenland. 3.3. Temporal trends All time trends have in common that they show decreasing concentrations of S6Toxaphene and individual congeners over time, with most decreases being statistically significant. Fig. 4 shows the time trend of S6Toxaphene for all sample types, and Table 2 summarises the trend statistics. Additional data and figures are available from the Supporting Information (Table S8; Figs. S4eS7). The overall decrease was expected, given the ban of toxaphene in the 1980s and the temporal development of other POPs banned t et al., 2010; in the same decade, for example that of PCBs (Rige Vorkamp et al., 2011; Dietz et al., 2013). The annual decrease of S6Toxaphene in adult ringed seals from East Greenland (4.5%) is comparable to that of S10-PCBs (3.4%), however, the study period is not identical (Vorkamp et al., 2011). Within the five sample types, the juvenile ringed seals from East Greenland showed the largest
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Fig. 4. Time trends of S6Toxaphene in Greenland. A: Arctic char (muscle). B: Juvenile ringed seals (blubber) from West Greenland. C: Juvenile ringed seals (blubber) from East Greenland. D: Adult ringed seals (blubber) from East Greenland. E: Black guillemot eggs. The filled dots are median values, the open circles are the individual values. The red line indicates a statistically significant trend. Blue stars are extreme values. Figures of individual toxaphene congeners are shown in the Supporting Information (Figs. S4eS7). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
annual change. Rather than biologically caused, this might be related to the longer time series dating back to 1986. Excluding the 1986 data point will still produce a significantly decreasing time trend for S6Toxaphene, however, the annual rate of decrease will be 6.5% instead of 7.2% (Table 2). As previously discussed for PCBs (Vorkamp et al., 2011), the main decrease might have taken place shortly after the ban in the 1980s and might not be caught by the time series starting around the year 2000. This could also be the reason for the non-significant decrease in the Arctic char time series, which started in 2004. From 1978 to 1988, toxaphene concentrations increased in walrus (Odobenus rosmarus rosmarus) from Greenland (Muir et al., 2000), which is consistent with the continued use of toxaphene until the late 1980s. A model of toxaphene accumulation in lake trout of the Great Lakes predicted the maximum concentration for the early 1980s, followed by a rapid and subsequently slowing decrease (Xia et al., 2011). The sediment core from Scotland indicated a peak for 1990 (Rose et al., 2001). These observations would be in line with maximum concentrations and the most rapid decline prior to our main monitoring period in Greenland starting around the year 2000. Regarding individual congeners, CHB 40 and CHB 41 were found to decrease significantly in Arctic char, at an annual rate of 17%
each (Table 2). As their contribution to S6Toxaphene is relatively small (Fig. 1B), this steeper decrease is not reflected in that of S6Toxaphene. In all sample types, CHB 40 and CHB 44 show the fastest decrease, while that of the most persistent congeners CHB 26 and CHB 50 was slowest. The time series for juvenile ringed seals from West Greenland and adult ringed seals from East Greenland cover the same time period and are very similar in the annual changes calculated for the individual congeners and S6Toxaphene (Table 2). They do not indicate major differences in the concentration developments at the west and east coast of Greenland although absolute levels are different (Fig. 2), probably a result of differences in air mass transport and thus, wildlife exposure as discussed above. A time trend for juvenile seals in West Greenland had been analysed previously (Vorkamp et al., 2008), covering the years 2000e2006. The extension to 2012 has sharpened the results for this time series: While the earlier trend of S6Toxaphene was nonsignificant, with an annual change of 4.3%, the updated trend is now statistically significant (p < 0.01) and gives an annual change t et al. (2010) analysed the statistical power of time of 5.2%. Rige series, in the context of their length, the number of samples per year, the random year to year variation, the significance level and the change to be detected. Within the Arctic Monitoring and
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Table 2 P-values for linear and non-linear trend components for Arctic char, juvenile ringed seals (4 years) from West Greenland as well as juvenile ringed seals (4 years), adult ringed seals and black guillemot eggs from East Greenland. F-values and residuals of the log-linear test are given in the Supporting Information. Congener
Time period
Log-linear trend component Annual change (%)
Non-linear trend component p-values
Arctic char (muscle)a CHB-26 2004e2012 0.8 0.84 CHB-40 2004e2012 17.1 <0.01 CHB-41 2004e2012 16.7 <0.01 CHB-44 2004e2012 11.5 0.16 CHB-50 2004e2012 3.7 0.54 CHB-62 2004e2012 10.0 0.52 2004e2012 4.9 0.38 S6Toxaphene Juvenile ringed seal (4 years) (blubber), Central West Greenland CHB-26 2000e2012 4.2 0.02 CHB-40 2000e2012 11.5 <0.01 CHB-41 2000e2012 8.0 <0.01 CHB-44 2001e2012 11.4 <0.01 CHB-50 2000e2012 6.7 <0.01 CHB-62b 2000e2012 e e S6Toxaphene 2000e2012 5.2 <0.01 Juvenile ringed seal (4 years) (blubber), Central East Greenland CHB-26 1986e2012 3.0 <0.01 CHB-40 1986e2012 10.9 <0.01 CHB-41 1986e2012 10.5 <0.01 CHB-44 2001e2012 10.4 <0.01 CHB-50 1986e2012 5.5 <0.01 CHB-62c 1986e2012 9.6 <0.01 S6Toxaphene 1986e2012 7.2 <0.01 Adult ringed seal (>4 years) (blubber), Central East Greenland CHB-26 2000e2012 4.3 0.06 CHB-40 2000e2012 11.7 <0.01 CHB-41 2000e2012 8.5 0.01 CHB-44 2001e2012 18.4 <0.01 CHB-50 2000e2012 5.6 0.01 CHB-62d 2000e2012 5.9 <0.01 S6Toxaphene 2000e2012 4.5 0.20 Black guillemot eggs, Central East Greenland CHB-26 1999e2012 2.1 0.32 CHB-40 1999e2012 7.1 <0.01 CHB-41 1999e2012 3.8 0.18 CHB-44 1999e2012 8.3 0.02 CHB-50 1999e2012 4.0 0.10 CHB-62 1999e2012 7.6 0.20 S6Toxaphene 1999e2012 4.7 0.03
p-values
e e e e e e e 0.07 0.17 0.09 0.02 0.12 e 0.12 0.04 1.0 1.0 0.04 0.02 0.24 0.19 0.14 0.15 0.15 0.28 0.18 0.02 0.68 0.62 1.0 0.46 0.63 0.57 0.38 1.0
a
The number of years did not allow test of the non-linear trend component. No time trend analysis possible because only data from 2006 and 2010 had a median above detection limits. c Data did not allow median calculations in 2001 and 2002. d Data did not allow median calculation in 2002. b
Assessment Programme (AMAP) only 8% of the time series had a statistical power of 80% to detect an annual change of 5% at a significance level of 5%. Based on these analyses, the authors concluded that more than 10 years of data were required before sufficient statistical power was obtained to detect significant cont et al., 2010). This agrees centration changes in the time series (Rige with the results of this study, which only showed significant trends for ringed seals and black guillemot eggs, i.e. the longest time series. Time trends in ringed seals were also studied at four locations in the Canadian Arctic, but none of the time series showed a significant trend (Muir et al., 2013). This is unexpected as these time series also date back to the 1980s, however, they generally include only few data points prior to 2005. Interestingly, increasing concentrations have been observed in the more recent measurements (Muir et al., 2013), dividing the overall time trend into two phases.
Other time trend studies from the Arctic have mainly focussed on freshwater fish. Lake trout (Salvelinus namaycush) and burbot (Lota lota) were studied in three lakes of the Yukon Territory, Canada from 1993 to 2003 (Ryan et al., 2005), however, with inconclusive results: Toxaphene decreased in lake trout muscle, but not in burbot liver for which a >200% increase was observed in Lake Quiet. An update focussing on Lake Laberge did show significantly decreasing concentrations of toxaphene in lake trout, burbot and several other freshwater species. However, growth dilution and changes in ecosystem structures might have affected the organochlorine concentrations (Ryan et al., 2013). Updates from 2011 confirmed decreasing concentrations of toxaphene in lake trout from Lake Laberge, while no new data were available for burbot (Muir et al., 2013). Besides the Yukon lakes, temporal trends of toxaphene in the freshwater environment of the Canadian Arctic were studied for lake trout and burbot from the Great Slave Lake, sea-run Arctic char at two locations, burbot in the Mackenzie River and landlocked Arctic char in four lakes of the high Arctic (Muir et al., 2013). In agreement with observations for ringed seals, some of these time series showed recent or temporary increases of toxaphene, for example, toxaphene in burbot from the Mackenzie River was found to increase from 2001 to 2009, and then returned to the 2001 level. An upward trend was also observed in landlocked Arctic char between 2003 and 2010, which the authors attributed to mobilisation of old sources in the area. However, the trends including samples from the 1990s generally showed lower concentrations in recent measurements. Peregrine falcon eggs (Falco peregrinus) collected in Greenland between 1986 and 2003 did not show any significant trends for S6Toxaphene or individual congeners (Vorkamp et al., 2014). Using the same approach as in this study, four congeners showed a nonsignificant positive trend, while only CHB 26, CHB 40 and S6Toxaphene showed a decreasing, but non-significant trend. These results were different from those of chlordane-related pesticides in the same samples, a compound group with a similar phase out history, but lower production volumes than toxaphene. The authors discussed that secondary sources of toxaphene in combination with a long life span of the peregrine falcons might have caused their exposure. Outside the Arctic, overall decreases of toxaphene were found for fish of the Great Lakes, for which toxaphene concentrations were monitored from 1989 to 2009 (Chernyak et al., 2005; Glassmeyer et al., 1997; Hickey et al., 2006; Xia et al., 2012). Decreases of toxaphene were also observed in beluga (Delphinapterus leucas) from the St. Lawrence River in Canada, during the period 1988e1999 (Gouteux et al., 2003). The authors remarked that the decrease by approximately a factor of 2 was comparable to the emission reductions in the Southern United States. In Europe, toxaphene levels in eggs of tawny owl from Norway decreased by a factor of 4 from the first study period (1986e1995) to the second one (1998e2004), while no trend was found in black guillemot muscle collected in Iceland between 1977 and 1992 (Olafsdottir et al., 2005). In summary, there is evidence of decreasing concentrations of toxaphene in most species and study areas although species from the marine environment have been studied to a lesser extent. Few exceptions from the overall decreases exist, which might be related to the time period covered by the time trend study and thus the power of the time series. Furthermore, ecological factors, such as varying feeding behaviour, might play a role in these observations, as well as exposure to newly released toxaphene from secondary sources.
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4. Conclusions Toxaphene accumulates strongly in black guillemot eggs, but seems to undergo transformation in ringed seals, with consequences of a lower exposure to polar bears compared with other POPs. Although toxaphene follows the East Greenland > West Greenland pattern observed for other POPs, its circumpolar trend is different. Highest concentrations occur in the North American Arctic, probably a result of the main use of toxaphene in the USA. Toxaphene concentrations have been decreasing in Arctic char, black guillemot eggs and ringed seals from Greenland, which supports time trend studies of other species and in other regions. Observations in the Canadian Arctic of recent toxaphene increases are not apparent in the Greenland time series as of 2012. Acknowledgements The study was funded by the Danish Cooperation for Environment in the Arctic (DANCEA) of the Danish Environmental Protection Agency. The authors wish to thank Derek Muir for help with Fig. 3 and Sigga Joensen, Annegrete Ljungqvist and Birgit Groth for technical assistance in the laboratory. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2015.02.014. References ATSDR, 2010. Draft Toxicological Profile for Toxaphene. U.S. Department of Health and Human Services. Public Health Service. Agency for Toxic Substances and Disease Registry. Berntssen, M.H.G., Lundebye, A.-K., Hop-Johannessen, L., Lock, E.-J., 2012. Dechlorination of the dietary nona-chlorinated toxaphene congeners 62 and 50 into the octa-chlorinated toxaphene congeners 44 and 40 in zebrafish (Danio rerio) and Atlantic salmon (Salmo salar). Aquat. Toxicol. 112e113, 54e61. Bidleman, T.F., Falconer, R.L., Wallab, M.D., 1995. Toxaphene and other organochlorine compounds in air and water at Resolute Bay, N.W.T., Canada. Sci. Total Environ. 160/161, 55e63. Braekevelt, E., Tomy, G.T., Stern, G.A., 2001. Comparison of an individual congener standard and a technical mixture for the quantification of toxaphene in environmental matrices by HRGC/ECNI-HRMS. Environ. Sci. Technol. 35, 3513e3518. Braune, B.M., Simon, M., 2004. Trace elements and halogenated organic compounds in Canadian Arctic seabirds. Mar. Poll. Bull. 48, 986e1008. Breivik, K., Sweetman, A., Pacyna, J.M., Jones, K.C., 2002. Towards a global historical emission inventory for selected PCB congeners e a mass balance approach: 1. Global production and consumption. Sci. Total Environ. 290 (1e3), 181e198. Bustnes, J.O., Yoggoz, N.G., Bangjord, G., Polder, A., Skaare, J.E., 2007. Temporal trends (1986-2004) of organochlorines and brominated flame retardants in tawny owl eggs from Northern Europe. Environ. Sci. Technol. 41, 8491e8497. Chernyak, S.M., Rice, C.P., Quintal, R.T., Begnoche, L.J., Hickey, J.P., Vinyards, B.T., 2005. Time trends (1983-1999) for organochlorines and polybrominated diphenyl ethers in rainbow smelt (Osmerus mordax) from Lakes Michigan, Huran, and Superior, USA. Environ. Toxicol. Chem. 24 (7), 1632e1641. de Boer, J., Wester, P.G., 1993. Determination of toxaphene in human milk from Nicaragua and in fish and marine mammals from the Northeastern Atlantic and the North Sea. Chemosphere 27 (10), 1879e1890. de Geus, H.-J., Besselink, H., Brouwer, A., Klungsøyr, J., McHugh, B., Nixon, E., Rimkus, G.G., Wester, P.G., de Boer, J., 1999. Environmental occurrence, analysis, and toxicology of toxaphene compounds. Environ. Health Persp. 107 (Suppl. 1), 115e144. Dietz, R., Heide-Jørgensen, M.-P., Harkonen, T., Teilmann, J., Valentin, N., 1991. Age determination in European harbour seals Phoca vitulina L. Sarsia 76 (1e2), 17e21. t, F.F., Sonne, C., Born, E.W., Bechshøft, T., McKinney, M.A., Letcher, R.J., Dietz, R., Rige 2013. Three decades (1983e2010) of contaminant trends in East Greenland polar bears (Ursus maritimus). Part 1: legacy organochlorine contaminants. Environ. Int. 59, 485e493. Fisk, A.T., Rosenberg, B., Cymbalisty, C.D., Stern, G.A., Muir, D.C.G., 1999. Octanol/ water partition coefficients of toxaphene congeners determined by the “slowstirring” method. Chemosphere 39 (14), 2549e2562. Føreid, S., Rundberget, T., Severinsen, T., Wiig, Ø., Skaare, J.U., 2000. Determination of toxaphenes in fish and marine mammals. Chemosphere 41, 521e528. Glasius, M., Christensen, J.H., Platz, J., Vorkamp, K., 2005. Halogenated organic
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