Temporal Dynamics of Circulating Persistent Organic Pollutants in a

Article pubs.acs.org/est

Temporal Dynamics of Circulating Persistent Organic Pollutants in a Fasting Seabird under Different Environmental Conditions Jan Ove Bustnes,*,† Børge Moe,† Sveinn Are Hanssen,† Dorte Herzke,‡ Anette A. Fenstad,§ Tore Nordstad,∥ Katrine Borgå,⊥ and Geir W. Gabrielsen∥ †

Norwegian Institute for Nature Research, FRAM − High North Research Centre on Climate and the Environment, NO-9296 Tromsø, Norway ‡ Norwegian Institute for Air Research, FRAM − High North Research Centre on Climate and the Environment, NO-9296 Tromsø, Norway § Department of Biology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway ∥ Norwegian Polar Institute, FRAM − High North Research Centre on Climate and the Environment, NO-9296 Tromsø, Norway ⊥ Norwegian Institute for Water Research, Gaustadalléen 21, NO-0349 Oslo, Norway S Supporting Information *

ABSTRACT: Temporal dynamics of persistent organic pollutants (POPs) were examined in fasting common eider (Somateria mollissima) females in one subarctic (68° N; over 5 years) and one high arctic colony (78° N; 3 years). Blood concentrations of polychlorinated biphenyl (PCB)-153; 1-dichloro-2,2-bis (p-chlorophenyl) ethylene (p,p′-DDE), and hexachlorobenzene (HCB) were measured twice each season in eider females (total n = 162) during incubation (at day 5 and day 20). The mean wet weight concentrations of PCB-153 were ∼3−5 times higher in the subarctic colony, whereas p,p′-DDE and HCB concentrations tended to be higher in high arctic than in subarctic eiders late in the incubation period. All POPs increased during incubation fast, but the relative increase in mean concentration varied more among years in high arctic than in subarctic eiders. In the high arctic, both lipid-metabolism and the increase in circulating POP concentrations were highest in the year when the mean ambient temperature was lowest. Moreover, females with low body condition and high lipid metabolism (body mass loss) had stronger increase in circulating concentrations of p,p′-DDE and HCB; the effect size being within the same order of magnitude in the two colonies. Hence, since eiders at high latitudes metabolized relatively more lipids, they experienced higher exposure of p,p′-DDE and HCB over the incubation period than birds inhabiting the more benign subarctic region.

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INTRODUCTION Evidence is mounting that climate may directly or indirectly interfere with the exposure of lipid-soluble persistent organic pollutants (POPs) in wildlife, and climate change has become an important issue in ecotoxicology.1−3 However, there are different mechanisms through which climate may influence POP concentrations and composition in animals. For example, changes in winds and oceanic currents may directly increase or decrease the transport of POPs to remote locations with subsequent biomagnification in food chains.1,4 There might also be changes in species compositions and food web structures in ecosystems making predators alter their diet, and thereby their uptake of POPs.5,6 Furthermore, climate may impact organisms more directly through changes in temperatures. For example, at low temperatures many species depend on metabolizing stored body fat reserves which lead to remobilization of lipid-soluble POPs and increased circulating concentrations.7−13 In the arctic glaucous gull (Larus hyperboreus), Henriksen et al.9 found that a © 2012 American Chemical Society

100 g reduction in body fat reserves (5−10% of body mass) led to a doubling of blood concentrations of some organochlorines (OCs). In fasting birds, circulating concentrations are expected to increase even more as nearly all lipid reserves may be mobilized. Moreover, it is advantageous to study fasting animals when evaluating how various predictors may influence circulating concentrations of lipid-soluble POPs, since feeding will interfere with both lipid-content and concentrations of POPs in the blood, and also body burden of POPs. The common eider (Somateria mollissima; denoted eider) is a largebodied marine duck (2−3 kg) where females accumulate large lipid reserves prior to breeding. During egg laying and incubation fast (3.5−4 weeks) they may lose as much as 30− Received: Revised: Accepted: Published: 10287

May 2, August August August

2012 13, 2012 21, 2012 31, 2012

dx.doi.org/10.1021/es301746j | Environ. Sci. Technol. 2012, 46, 10287−10294

2005 body mass lipid% PCB-153 p,p′-DDE HCB 2006 body mass lipid% PCB-153 p,p′ -DDE HCB 2007 body mass lipid% PCB-153 p,p′-DDE HCB 2008 body mass lipid% PCB-153 p,p′ -DDE HCB 2009 body mass lipid% PCB-153 p,p′ -DDE HCB

1985

784.3 349.2 358.8

17 17 17 17 17

13

13 13 13

(g)

10288

(g)

1884 0.06 639.0 265.8 168.5

1928 0.25 911.9 355.8 221.3

9 9 9 9 9

(g)

2028 0.09 527.1 266.1 215.4

1754 193.1 922.0

10 10 10

10 10 10 10 10

2007

10

mean

(g)

(g)

n

670.7 362.0 354.0

2010

1880 0.05 541.6 194.9 145.0

1920 0.23 841.7 332.3 225.1

1995 0.09 370.7 165.7 160.0

1140 20.13 895.0

2005

median

392.8 249.2 132.7

126.1

159.3 0.04 413.4 199.9 83.76

78.70 0.07 802.9 377.2 75.77

103.258 0.04 413.8 275.4 130.6

1336 371.0 469.4

128.2

SD

first measurement (day 5)

1454.2 684.3 704.1

1585

1559 0.15 2019 683.6 295.6

1549 0.30 2864 1249 422.1

1656 0.11 1161 692.9 305.9

3480 1046 1370

1620

mean

1459 644.2 756

1570

1540 0.16 1638 655.7 289.1

1530 0.25 2691 1305 359.6

1640 0.10 969.3 510.6 232.0

3150 860.0 1300

1610

median

708.8 452.4 179.6

111.6

137.6 0.05 1338 397.1 140.3

71.67 0.14 1415 653.1 151.1

89.09 0.04 805.2 595.3 205.6

2253 687.8 593.1

115.9

SD

second measurment (day 20)

subarctic (68° N)

669.8 335.1 304.9

400.0

324.1 0.09 1380 417.7 127.1

378.9 0.05 1952 893.2 200.8

372.0 0.02 634.3 426.8 90.44

1726 857.0 448.0

387.0

mean change

46.20 23.65 21.25

27.94

99.47 29.18 9.03

23.41

124.3 56.96 12.95

24.64

41.91 28.60 5.74

24.79

119.8 58.38 31.65

27.01

mean daily change

23 23 23

23

38 38 38 38 38

42 42 42 42 42

n

247.3 362.6 387.9

1799

1833 0.07 106.3 156.6 129.3

1781 0.22 190.6 189.7 336.3

mean

202.4 251.6 336.1

1836

1809 0.07 76.9 131.2 97.5

1784 0.22 166.6 91.5 273.2

median

first measurement

144.7 367.7 172.6

106.8

139.7 0.04 180.2 174.9 83.48

118.6 0.09 167.3 211.6 225.5

SD

640.1 952.8 669.0

1421

1406 0.21 1062 750.9 559.2

1430 0.29 693.3 1517 582.1

mean

485.0 402.7 601.4

1430

1401 0.20 653.8 536.9 488.0

1427 0.29 557.7 1265 543.7

median

606.7 1902 220.6

89.63

116.1 0.12 1084 735.5 490.8

98.44 0.09 373.6 893.5 235.2

SD

second measurment

high arctic (78° N)

392.8 590.2 281.1

377.2

427.5 0.14 923.8 585.1 350.6

351.3 0.07 502.7 1327 245.8

mean change

26.49 40.67 18.73

25.32

62.01 38.43 27.88

27.68

33.21 87.50 16.07

23.11

mean daily change

Table 1. Body Mass, Lipid Content in the Blood (%), and Concentrations of PCB-153, p,p′-DDE, and HCB (pg/g Wet Weight) in Common Eider Females Early (Day 5) and Late (Day 20) in the Incubation Period in One Subarctic (Northern Norway) and One High Arctic (Svalbard) Colony in Different Years

Environmental Science & Technology Article


Environmental Science & Technology

Article

variation in DLs between years and compounds we standardized the nondetects to half of the highest DL in the analyses of the different years (40.25 pg/g wet weight = 20.125). Lipid content in the blood samples was determined gravimetrically. Data on lipid content in the blood were, however, lacking from Grindøya in 2005, and due to a laboratory problem no samples from 2009 could be analyzed for lipid content. Data Analyses. Statistical analyses were carried out using SAS 9.327 and the R system.28 First, we excluded those individuals for which both day 5 and day 20 measurements of one or more POPs were below detection, because the rate of change could not be assessed. Second, a number of individuals were sampled in more than one year, and to achieve independence among the samples we kept only one of those observations; i.e. the observation from the year with the smallest sample size. Furthermore, when testing the effects of different predictors on the changes in POP concentrations we limited the samples to those individuals for which we had measurements for all predictors (2006−2008 for the subarctic colony and 2007−2008 for the high arctic), to enable us to compare the three compounds within and between locations. Since there was some variation in the number of days between the two samplings, the daily change of the three POPs (i.e., pg/ g, wt. weight: [concn 2 − concn 1]/no. days between) were used as dependent variables. The main predictors of interest were the body condition at the first POP measurement (body mass at day 5) and amount of body mass loss (changes in the body weight (g) between first and second sampling). We also controlled for the following covariables in the models: year (as a discrete variable), initial level of the contaminant in question, blood lipid (%) at day 5, and changes in blood lipid between first and second sampling. Before analyses the data set was checked for outliers: one individual for the high arctic colony had extremely low body mass loss; for changes in blood lipids there were three extreme individuals (one for the high arctic and 2 for the subarctic colony); finally there was one outlier for daily change in PCB-153 in the high arctic colony. Overall the data set consisted of 162 individuals (Table 1). Before statistical modeling it was necessary to transform the daily changes in PCB-153 concentrations (log) and p,p′-DDE (square root) for the high arctic birds to meet assumptions of normality and constant variance. To estimate the effect sizes, we back-transformed the model estimates. No transformations were necessary for the subarctic colony or for HCB in the high arctic colony.The goodness of fit of linear models was assessed using partial residual plots and influence values.29 We evaluated different models based on Akaike’s Information Criteria (AIC), corrected for small sample size (AICc),30 to assess the effects of each predictor of interest. More specifically we calculated the relative likelihood of each model using AICc weights derived from difference in AICc values between the best model (lowest AICc) and other models.30,31 We used variable importance (sum of AICc weights of all models including this variable) to assess the robustness of the model selection procedure.31 We provide the statistics for the five best models for each compound (see Supporting Information (SI) Tables 1 and 2).

45% of their initial body mass, mostly through lipid metabolism.14−19 In addition there is great seasonal variation in POP concentrations in common eiders,20,21 and in high arctic eiders, mean blood concentrations of polychlorinated biphenyl (PCB)-153, 1,1-dichloro-2,2-bis (p-chlorophenyl) ethylene (p,p′-DDE), and hexachlorobenzene (HCB) increased 2−8 fold during incubation.13 Here we analyzed the dynamics of POPs in blood of eiders breeding in both a subarctic region (northern Norway) and in the high arctic (Svalbard), over several years. Due to the proximity to POP sources, we expected higher concentrations of POPs in the subarctic birds compared to the high arctic, especially of heavily chlorinated compounds with relatively low transport potential.22 Furthermore, we hypothesized that eiders breeding in the high arctic, where summer temperatures are consistently lower than in the subarctic, would metabolize relatively more of their body lipids during their incubation fast. Hence, because of equilibrium partitioning of POPs among adipose tissue and blood, high arctic eiders would experience greater remobilization of POPs than birds from the more benign subarctic environments. Implicitly, there should be associations between body condition and the amount of lipid metabolized, and the magnitude of changes in POP concentrations over the fasting period.13 By sampling blood twice from the same female eiders within seasons in one subarctic (5 years) and one high arctic (3 years) colony, we examined the spatial and temporal variation in the build-up of PCB-153, p,p′-DDE, and HCB in blood over a 15day incubation period.

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MATERIALS AND METHODS In the high arctic, the study was carried out at Storholmen in Kongsfjorden, Svalbard (78°56′ N, 12°13 E), between 2007 and 2009. This island has a breeding population of 500−1000 pairs of common eiders, varying between years (G.W. Gabrielsen, unpublished data). The average temperature in Kongsfjorden in June, when eiders incubate, is 2.5 °C. In the subarctic region we studied a colony on Grindøya near Tromsø (69°39′ N, 18°57′ E) in northern Norway between 2005 and 2009. At Grindøya, about 200−300 pairs of eiders may breed.23,24 The average temperature in Tromsø in June is 8 °C. Eider nests were marked at the start of egg laying and followed until hatching. The nests were checked during the egg laying period, with a 3-day interval, and new eggs were recorded. The females were caught and blood was sampled both 5 and 20 days after the egg laying was completed (incubation is initiated just before the last egg is laid).25 Some individuals were, however, impossible to catch at the preset date (day 5 or day 20) and thus the number of days between sampling varied between 9 and 19 (x̅ = 14.3 ± 1.7 SD) for Grindøya, and 13 and 17 (x̅ = 15.3 ± 0.8 SD) for Storholmen. A blood sample of ca. 10 mL was taken from the jugular vein with a syringe. Body mass was recorded using a spring balance. Data on temperatures was retrieved from the Norwegian Meteorological Institute at www.eklima.met.no. Chemical Compounds and Analyses. The chemical analyses were carried out at the Norwegian Institute for Air Research (NILU) in Tromsø. A thorough description of the POP analyses can be found in Bustnes et al.13,26 PCB-153, p,p′DDE, and HCB (wet weight [pg g−1, ww] concentrations) were selected because they were found in high concentrations (>75% above detection limits [DLs]) and because they represent somewhat different physiochemical properties, especially with regard to volatility and long-range transport potential.22 Due to

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RESULTS AND DISCUSSION Spatial and Temporal Variation in Lipid Dynamics and POP Concentrations. The mean body mass was higher in the subarctic eiders compared to the high arctic eiders (Table 1), both at day 5 and day 20 (P < 0.0001; test for all years combined and controlled for incubation stage). Over all years, 10289



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the daily weight loss of high arctic and subarctic eiders was the same (25.3 vs 25.4 g/day, respectively; P = 0.79). However, high arctic eiders lost weight at a significantly higher rate than subarctic eiders (1.44% vs. 1.32% of initial body mass per day, respectively; P = 0.0001). The body mass loss in the high arctic differed among years (P < 0.0001) and was highest in the coldest year; 2008 (Table 1) when mean ambient temperature during incubation was 1.5 °C, compared to 2.4 and 3.6 °C in 2007 and 2009, respectively. In the subarctic colony there were also differences in the daily rate of body mass loss among years (P < 0.02, Table 1), also being highest in the coldest year: i.e. 2009 when mean temperature in June was 7.1 °C. The lower critical temperature in arctic eiders has been found at 7 °C, below which females need to increase their energy expenditure to maintain normal body temperature.16 Hence, ambient temperature seems to be a more important factor determining the rate of lipid metabolism in high arctic eiders compared to eiders in the subarctic region, where mean temperature in June is ∼8 °C. Actually, based on the temperature differences between the two areas one might expect greater differences in lipid mobilization. However, eiders have well insulated nests which might mitigate the effect of low temperatures during incubation. The lipid content in the blood varied significantly between years in both locations both at day 5 and day 20 (P < 0.0001, Table 1). Moreover, the amount of lipids was higher at day 20 compared to day 5 in both colonies, significantly for 2008 in the subarctic (P = 0.0003) and for both years in the high arctic (P < 0.0001, Table 1). The concentrations of PCB-153 were highest in the subarctic eiders, both at day 5 and day 20 (Table 1; P < 0.0001: all years combined). In the high arctic, HCB concentrations were significantly lower at day 5 compared to the subarctic (P = 0.045), but tended to be higher at day 20 (Table 1), although not significant (P = 0.14). This is in general in agreement with previous studies showing that heavy chlorinated PCB congeners with low transport potential occur in higher concentrations closer to their sources, whereas the lighter and more volatile HCB is relatively higher in remote areas such as the Arctic.22 Overall, p,p′-DDE concentrations were not significantly different between the colonies (P > 0.38), although the high arctic colony tended to be higher at day 20 (Table 1). The relatively high p,p′-DDE concentrations in the high arctic might depend on continued use of DDT in some parts of the world, and potential transport to remote areas.32 It has also been suggested that p,p′-DDE loads will increase in polar environments as glaciers melt because relatively more of DDT is embedded in the ice.1,33 Such processes may lead to annual variation in the inputs of p,p′-DDE to the northern benthic communities, where eiders feed. In the subarctic colony the relative increase in mean concentrations of PCB-153 and HCB between day 5 and day 20 was relatively moderate and stable over the five years (2−3 and 1.4−2 fold increase, respectively), whereas p,p′-DDE was more erratic (2−5 fold increase) (Figure 1). In the high arctic colony, however, the annual variations for all compounds were greater; i.e. 2−10 fold increase for PCB-153 concentrations, 2.6−8 folds for p,p′-DDE, and 1.7−4 fold for HCB (Figure 1). Moreover, in the high arctic the increase in PCB-153 and HCB was highest in 2008 (Figure 1) which could be predicted from the high rate of lipid metabolism (Table 1). In terms of absolute concentrations, the mean daily rate of increase was much higher in the subarctic compared to the high arctic

Figure 1. Relative increase in mean blood concentrations of three persistent organic pollutants between day 5 and day 20 during incubation in fasting common eider females in different years in one high arctic (Svalbard) colony and subarctic (northern Norway) colony.

colony for PCB-153 (82.2 vs. 42.3 pg/day, respectively; P < 0.0001 all years combined, Wilcoxon two-sample test), whereas the situation was reversed for both p,p′-DDE (58.9 vs. 37.05 pg/day; P = 0. 1) and HCB (21.0 vs. 15.6 pg/day; P < 0.0028). Hence, eiders in the high arctic experienced a more rapidly increasing exposure of p,p′-DDE and HCB than the subarctic eiders. Effects of Lipid Dynamics on the Remobilization of POPs. The partition of lipid-soluble POPs between blood and tissue is mainly determined by lipid content in different compartments and concentration gradients,34,35 and in birds the concentrations in active adipose tissue are normally positively associated with the circulating concentrations.9,36−38 10290



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Figure 2. Predicted changes in blood concentrations of three persistent organic pollutants (pg/g per day) in fasting common eiders breeding in a subarctic (left column) and a high arctic (right column) colony, as a function of initial body mass (g: controlled for different covariates in the best models which included initial body mass; see SI Tables 1 and 2, and SI Figures 1 and 2 for partial residual plots).

Hence, based on the equilibrium partitioning model,38 we predicted that lipid dynamics should be closely related to the changes in circulating POPs. The associations between the different predictors and the daily change in POP concentrations were similar in the high arctic (n = 80) and subarctic (n = 36) colonies, with some differences. For example, as could be expected from earlier bird studies,11,12,39 the changes in the blood lipids between day 5 and day 20 explained much of the changes of all compounds in the high arctic, but surprisingly not in the subarctic colony (SI Tables 1 and 2). However, in

the subarctic the content of lipids in the blood at day 5 was a significant explanatory variable for PCB-153 (SI Table 2). The reason for these colony differences is not known. Moreover, the best models explained more of the variation in the circulating concentrations for p,p′-DDE (46% vs. 23%) and HCB (45% vs. 9%) in the high arctic compared to the subarctic (SI Tables 1 and 2). For PCB-153 the situation was reversed and the predictors explained more of the variation in the subarctic (30%) compared to the high arctic (16%; SI Tables 1 and 2). 10291



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Figure 3. Predicted changes in blood concentrations of p,p′-DDE and HCB (pg/g per day) in fasting common eiders breeding in a subarctic (left column) and a high arctic (right column) colony, as a function of body mass loss (g) between incubation day 5 and day 20 (controlled for different covariates in the best models which included body mass loss; see SI Tables 1 and 2, and SI Figures 1 and 2 for partial residual plots).

The initial body condition (day 5) reflects the lipid reserves of eiders at the start of incubation, and it was negatively related to the daily increase of all three POPs in both colonies (Figure 2, SI Tables 1 and 2). However, the strength of the predicted effects varied among the compounds. For PCB-153 the effect of initial body mass was much stronger in the subarctic eiders compared to the high arctic birds and a 100 g lower initial body mass resulted in a predicted increase of 19 pg/g per day in subarctic eiders, whereas it was 5.5 pg/g in the high arctic eiders. This probably reflects the higher environmental contamination by PCBs closer to the sources. For both p,p′DDE and HCB, the effect of initial body mass was within the same order of magnitude in the two colonies (∼14 vs. 9.6 pg/g daily increase per 100 g decrease in body mass for p,p′-DDE, and ∼3.7 vs. 2.7 pg/g, for HCB, in the high arctic and subarctic colony, respectively; Figure 2). Furthermore, we also predicted that the amount of lipids metabolized (body mass loss) should be positively associated with increase in the blood contaminant concentrations, which was found in both colonies for p,p′-DDE (∼ 24 vs. 19 pg/g daily increase per 100 g increase in body mass loss in the subarctic and high arctic, respectively) and HCB (∼3.8 vs 8.4 pg/g; Figure 3). Based on the equilibrium partitioning model, the cause of the relationships among initial body mass, body mass loss, and changes in blood POPs is probably that birds with low body reserves have a larger fraction

of their total body lipid contained within the blood compared to adipose compartments. As they lose weight, the overall proportion of whole body lipids contained in blood increases faster for birds with low fat reserves compared to birds with high reserves. Likewise, the proportion of whole body lipids contained in adipose tissue decreases faster in birds with low fat reserves compared to fatter birds. This is probably why initial body weight had a stronger impact in the statistical models compared to the absolute weight loss experienced during incubation. However, initial body mass and amount of lipid loss may be dependent on one another considering it is the ratio of lipid content in blood to adipose tissue that is most important for driving blood concentrations and not absolute quantities of lipids in either compartment.38 This study thus showed some clear differences between high arctic and subarctic eiders, and between the different compounds. First, the proximity to sources was important for the heaviest chlorinated compound, PCB-153, whereas both p,p′-DDE and HCB tended to occur in higher concentrations in the high arctic, mainly as a result of higher increase over the incubation period (Table 1). Moreover, the annual variation in the circulating concentrations of POPs in incubating eiders, and that the high arctic colony showed greater variation than the subarctic colony, was consistent with influence of ambient temperature on the remobilization of POPs. This was 10292



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(6) Bustnes, J. O.; Yoccoz, N.; Bangjord, G.; Herzke, D.; Ahrens, L.; Skaare, J. U. Impacts of climate and feeding condition on the annual accumulation (1986−2009) of persistent organic pollutants in a terrestrial raptor. Environ. Sci. Technol. 2011, 45, 7542−7547. (7) Van den Brink, N. W.; van Franeker, J. A.; de Ruiter-Dijkman, E. M. Fluctuating concentrations of organochlorine pollutants during a breeding season in two Antarctic seabirds: adélie penguin and southern fulmar. Environ. Toxicol. Chem. 1998, 17, 702−709. (8) Henriksen, E. O.; Gabrielsen, G. W.; Skaare, J. U. Levels and congener pattern of polychlorinated biphenyls in kittiwakes (Rissa tridactyla) in relation to mobilization of body-lipids associated with reproduction. Environ. Pollut. 1996, 92, 27−37. (9) Henriksen, E. O.; Gabrielsen, G. W.; Skaare, J. U. Validation of the use of blood samples to assess tissue concentrations of organochlorines in glaucous gull Larus hyperboreus. Chemosphere 1998, 37, 2627−2643. (10) Bustnes, J. O.; Skaare, J. U.; Erikstad, K. E.; Bakken, V.; Mehlum, F. Whole blood concentrations of organochlorines as a dose metric for studies of the glaucous gull (Larus hyperboreus). Environ. Toxicol. Chem. 2001, 20, 1046−1052. (11) Bustnes, J. O.; Skaare, J. U.; Berg, V.; Tveraa, T. Inter-seasonal variation in blood concentrations of organochlorines in great blackbacked gulls (Larus marinus). Environ. Toxicol. Chem. 2005, 24, 1801− 1806. (12) Bustnes, J. O.; Tveraa, T.; Henden, J. A.; Varpe, Ø; Skaare, J. U. Organochlorines in antarctic and arctic avian top predators: a comparison between the south polar skua and two species of northern Hemisphere gulls. Environ. Sci. Technol. 2006, 40, 2826−2831. (13) Bustnes, J. O.; Moe, B.; Herzke, D.; Hanssen, S. A.; Nordstad, T.; Sagerup, K.; Gabrielsen, G. W.; Borgå, K. Strongly increasing blood concentrations of lipid-soluble organchlorines in high arctic common eiders during incubation fast. Chemosphere 2010, 79, 320−325. (14) Korschgen, F. P. Breeding stress of female eiders in Maine. J. Wildl. Manage. 1977, 41, 360−373. (15) Parker, H.; Holm, H. Patterns of nutrient and energy expenditure in female common eiders nesting in the high Arctic. Auk 1990, 107, 660−668. (16) Gabrielsen, G. W.; Mehlum, F.; Karlsen, H. E.; Andresen, Ø.; Parker, H. Energy cost during incubation and thremoregulation in the female common eider Somateria mollissima. Norsk Polarinst. Skrifter 1991, 195, 51−62. (17) Bolduc, F.; Guillemette, M. Incubation constancy and mass loss in the common eider Somateria mollissima. Ibis 2003, 145, 329−332. (18) Guillemette, M. Foraging before spring migration and before breeding in common eiders: does hyperphagia occur? Condor 2001, 103, 633−638. (19) Criscuolo, F.; Gabrielsen, G. W.; Gendner, J. P.; Le Maho, Y. Body mass regulation during incubation in female common eiders Somateria mollissima. J. Avian Biol. 2002, 33, 83−88. (20) Olafsdottir, K.; Skirnisson, K.; Gylfadottir, G.; Johannesson, T. Seasonal fluctuations of organochlorine levels in the common eider (Somateria mollissima) in Iceland. Environ. Pollut. 1998, 103, 153−158. (21) Mallory, M. L.; Braune, B. M.; Wayland, M.; Gilchrist, H. G.; Dickson, D. L. Contaminants in common eiders (Somateria mollissima) of the Canadian Arctic. Environ. Rev. 2004, 12, 197−218. (22) AMAP Assessment 2002; Persistent Organic Pollutants in the Arctic; Arctic Monitoring and Assessment Programme (AMAP): Oslo, Norway, 2004; Xvi + 310 pp. (23) Hanssen, S. A.; Folstad, I.; Erikstad, K. E. Reduced immunocompetence and cost of reproduction in common eiders. Oecologia 2003, 136, 457−464. (24) Hanssen, S. A.; Hasselquist, D.; Folstad, I.; Erikstad, K. E. Cost of reproduction in a long-lived bird: Incubation effort reduces immune function and future reproduction. Proc. R. Soc., Ser. B. 2005, 272, 1039−1046. (25) Hanssen, S. A.; Engebretsen, H.; Erikstad, K. E. Incubation start and egg size in relation to body reserves in the common eider. Behav. Ecol. Sociobiol. 2002, 52, 282−288.

supported by the fact that lipid dynamics were good predictors of the changes of these compounds over the course of incubation. This implies that high arctic eiders experience the highest concentrations of potential harmful contaminants, such as p,p′-DDE and HCB, at the end of the incubation period when they are in the poorest state.23,24 An important question arising from this research is how future warming of the arctic will affect the common eiders. If the temperature increases, we expect less lipid mobilization and hence less build-up of lipid soluble POPs in eider blood during the incubation. However, a changing climate will also affect the benthic food web on which the eiders totally depend for the build-up of necessary body reserves for reproduction, which again may reduce the initial body mass of eider females which the models show to be a strong factor affecting chemical mobilization rate. Finally, there may be other important differences between the eiders in the two regions than those discussed here (movement patterns, morphology, physiology, etc.), which might influence lipid metabolism and remobilization of POPs. Such questions may be addressed in future studies.

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ASSOCIATED CONTENT

S Supporting Information *

Statistical model selection tables and partial residual plots for the variables included in the best models, also showing data points. This information is available free of charge via the Internet at http://pubs.acs.org/.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We are grateful to the staff at Ny Ålesund research station (Kings Bay and Norwegian Polar Institute) for valuable support during field work, and three anonymous reviewers for comments that greatly improved the manuscript. We also thank Bård J. Bårdsen for statistical advice. The study was funded by the Norwegian Research Council through two International Polar Year projects (COPOL and Bird health) and by the Arctic field Grant.

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REFERENCES

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