Environmental Toxicology and Chemistry, Vol. 34, No. 7, pp. 1552–1561, 2015 # 2015 SETAC Printed in the USA

CIRCUMPOLAR CONTAMINATION IN EGGS OF THE HIGH-ARCTIC IVORY GULL PAGOPHILA EBURNEA MAGALI LUCIA,*y NANETTE VERBOVEN,y HALLVARD STRØM,y CECILIE MILJETEIG,z MARIA V. GAVRILO,xk BIRGIT M. BRAUNE,# DAVID BOERTMANN,yy and GEIR W. GABRIELSENy yNorwegian Polar Institute, Tromsø, Norway zDepartment of Biology, Norwegian University of Science and Technology, Trondheim, Norway xNational Park Russian Arctic, Archangelsk, Russia kJoint Directorate of Taimyr Nature Reserves, Norilsk, Russia #Environment Canada, National Wildlife Research Centre, Carleton University, Ottawa, Ontario, Canada yyDepartment of Bioscience, Arctic Research Centre, Aarhus University, Roskilde, Denmark (Submitted 15 September 2014; Returned for Revision 30 October 2014; Accepted 9 February 2015) Abstract: The ivory gull Pagophila eburnea is a high-Arctic species threatened by climate change and contaminants. The objective of the present study was to assess spatial variation of contaminant levels (organochlorines [OCs], brominated flame retardants [BFRs], perfluorinated alkyl substances [PFASs], and mercury [Hg]) in ivory gulls breeding in different areas across the Arctic region as a baseline for potential future changes associated with climate change. Contaminants were already determined in eggs from Canada (Seymour Island; except PFASs), Svalbard in Norway (Svenskøya), and 3 sites in Russia (Nagurskoe, Cape Klyuv, and Domashny). New data from Greenland allowed the investigation of a possible longitudinal gradient of contamination. The most quantitatively abundant OCs were p,p0 -dichlorodiphenyldichloroethylene (DDE) and polychlorobiphenyls. Mercury concentrations were higher in Canada compared with other colonies. Eggs from Nagurskoe often were characterized by higher OC and BFR concentrations. Concentrations gradually decreased in colonies situated east of Nagurskoe. In contrast, PFAS concentrations, especially perfluorooctanoate and perfluorononanoate, were higher in Greenland. Some of the contaminants, especially Hg and p,p0 -DDE, exceeded published thresholds known to disrupt the reproductive success of avian species. Overall, the levels of OCs, BFRs, and PFASs did not suggest direct lethal exposure to these compounds, but their potential synergetic/additive sublethal effects warrant monitoring. Environ Toxicol Chem 2015;34:1552–1561. # 2015 SETAC Keywords: Ivory gull

Perfluorinated alkyl substances

Persistent organic pollutants

Arctic

and PFAS contaminants, mercury (Hg) undergoes long-range atmospheric transport because of its highly volatile nature. Polar regions are therefore global sinks for this element as well [3]. The ivory gull is a high-Arctic species that spends the entire year in the north and is closely associated with sea ice. Three main wintering grounds were identified for northeast Atlantic populations (north Greenland, Svalbard, and Franz Josef Land) of this long-distant migrant species in southeast Greenland, along the Labrador sea-ice edge and in the Bering Strait region [9]. In Canada, where the status of the species was updated to “Endangered” in 2006, studies have claimed that 80% of the breeding population already has been lost during recent decades [10]. The ivory gull is considered endangered in most parts of its breeding range. Nevertheless, it is one of the most poorly known breeding birds in the northern hemisphere even though its high position in the marine food web makes this species particularly sensitive to contaminant exposure. Previous studies have demonstrated that this free-ranging Arctic species is indeed exposed to high contaminant concentrations along its distribution range in the Canadian, Norwegian, and Russian Arctic [11– 13]. These studies demonstrated in particular that the most quantitatively abundant legacy OCs found in the ivory gull eggs were p,p0 -dichlorodiphenyldichloroethylene (DDE) and sum polychlorobiphenyls (SPCBs). Previous studies demonstrated a clear west-to-east gradient in persistent halogenated organic contaminant concentrations in Arctic species, especially marine mammals [14]. For the ringed seal (Phoca hispida), this gradient of exposure ranged from low in Alaska and Western Canada to much higher in East

INTRODUCTION

The Arctic Region currently is undergoing dramatic changes, with temperatures increasing twice as fast as the global average and sea ice extent decreasing linearly by 3% to 7% per decade in the Arctic Ocean [1]. These climate-driven changes will have far-reaching effects on Arctic ecosystems. Two major anthropogenic drivers identified in the Arctic are climate change and long-range transported pollutants [2,3]. The Arctic acts as a sink for chemicals that are produced and released in industrialized parts of the world and transported northward by sea, air, and water masses, creating a truly global problem [4]. It has been predicted that climate change will have profound effects on contaminant pathways in this region through temperature increases, more low-pressure activity, increased river discharges and runoff from glaciers, and an accelerated rate of sea ice melting. These climate-related variables may influence the transport and thus the bioavailability of contaminants to Arctic biota [3]. Organohalogens of anthropogenic origin have been found in Arctic biota for decades [5,6]. Recently, new anthropogenic chemicals such as brominated flame retardants (BFRs) and perfluorinated alkyl substances (PFASs) have become widespread in the Arctic environment [7,8]. Both compounds, in addition to the established organochlorines (OCs), are of global environmental concern. In addition to BFR * Address correspondence to [email protected]. Published online 13 February 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/etc.2935 1552

Circumpolar contamination of the high-Arctic ivory gull

Greenland, Svalbard, Western Russia, and the Baltic region [14]. Polar bear (Ursus maritimus) populations from East Greenland and Svalbard also were distinguished by higher concentrations of dichlorodiphenyldichloroethane (DDT)-related compounds, nonachlors, oxychlordane, and higher-chlorinated and persistent PCB congeners (hepta- to nonachlorinated), compared with western locations in Alaska and Canada [15]. The objective of the present study, therefore, was to investigate a possible longitudinal gradient in OC, BFR, PFAS, and Hg concentrations in the eggs of ivory gulls. Seabird eggs are useful monitoring tools, because they reflect the contaminant burden of the females that laid them [16]. To this end, newly acquired contaminant concentrations in ivory gull eggs from Station Nord, Greenland, were compared with previously published data obtained in 5 other colonies situated along the circumpolar distribution of the species in the Canadian (Seymour Island), Norwegian (Svalbard, Svenskøya), and Russian Arctic (Nagurskoe and Cape Klyuv in Franz Josef Land and Domashny Island in Severnaya Zemlya archipelago) [11–13]. MATERIALS AND METHODS

Sample collection and preparation

Eggs were collected at Station Nord, Greenland (818610 N, 168590 W; n ¼ 10) in 2010 and compared with eggs previously collected from Seymour Island, Nunavut, Canada (768480 N, 1018160 W; n ¼ 6) in 2004; from Svenskøya, Svalbard (788470 N, 268360 E; n ¼ 10) in 2007; and from Nagurskoe (808480 N, 478370 E; n ¼ 6) and Cape Klyuv (818390 N, 628110 E; n ¼ 7) in Franz Josef Land and Domashny (798300 N, 918050 E; n ¼ 12) in Severnaya Zemlya, northwestern Russia in 2006 (Figure 1). In Svalbard, Greenland, Franz Josef Land, and Severnaya Zemlya, 1 egg was sampled from each nest. To minimize disturbance of the nesting birds, egg laying sequence was not determined, and eggs were taken randomly from each nest. Measurement and incubation stage were not recorded for all colonies and eggs, and no attempt was made to adjust for moisture loss. However, we are unaware of any desiccated eggs. The eggs were wrapped individually in aluminum foil and stored frozen in separate plastic bags until further analyses. To

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prepare the samples, eggshells were removed thoroughly, and the whole egg content (including the embryo when present) was homogenized individually using a food blender (Melissa, Adexi Group, or Waring Commercial Laboratory Blender, Waring Laboratory). The homogenates were separated into aliquots for different analyses and stored at –20 8C until laboratory analysis. Eggs collected from Seymour Island were kept cool in the field and shipped to the National Wildlife Research Centre for processing and archival. Egg contents were then homogenized and stored frozen (–40 8C) in acetone–hexane rinsed glass vials [12,13]. Determination of OCs and BFRs in eggs from Svalbard, Greenland, Franz Josef Land, and Severnaya Zemlya

The chemical analyses of OCs and BFRs in eggs from Svalbard and both Russian archipelagos were described previously in Miljeteig et al. [11]. For the present study, the same methods were employed to analyze eggs from Greenland. All analyses were conducted at the accredited (TEST 137, NSEN ISO/IEC, 17025) Laboratory of Environmental Toxicology at the Norwegian School of Veterinary Science in Oslo, Norway. Egg homogenates were spiked with internal standards. Lipids were extracted twice using cyclohexane and acetone, and lipid content was determined gravimetrically. The extract was treated twice with ultra clean (purity 98.8%) concentrated H2SO4 (Scanpure, Chemscan) for sample clean up. An aliquot for toxaphene analyses required further separation on silica column. The extract was shaded from ultraviolet light exposure during the analytical process to prevent degradation of BFRs. All glassware was washed with cyclohexane:acetone (1:1) prior to use. Separation and quantification of the organic compounds was performed by high-resolution gas chromatographs (Agilent 6890 Series; Agilent Technologies) coupled to a mass spectrometer (MS; Agilent 6890 Series; Agilent Technologies) for BFRs, toxaphenes (chlorobornanes; CHB), and mono-ortho PCBs or to an electron capture detector (Agilent 5673; Agilent Technologies) for organochlorine pesticides and PCBs. Detection limits for individual compounds were determined as 3 times the baseline noise level and ranged from 0.12 ng g1 to 0.68 ng g1 wet weight for the organochlorine pesticides, from 0.20 ng g1 to 0.44 ng g1 wet weight for the PCBs, from 0.20 ng g1 to 1.00 ng g1 wet weight for the mono-ortho PCBs, and from 0.01 ng g1 to 0.30 ng g1 wet weight for the BFRs. Blank samples were below the detection limit for all reported analytes, and recovery and reference samples were deemed acceptable within 2 times the standard deviation (SD). Determination of OCs and BFRs in eggs from Seymour Island

Figure 1. Map of the circumpolar sampled colonies of the ivory gull in Seymour Island (Canada), Station Nord (Greenland), Svenskøya (Svalbard, Norway), and Nagurskoe and Cape Klyuv in Franz Josef Land and Domashny Island in Severnaya Zemlya (western Russian Arctic).

In Canada, egg homogenates were analyzed as pooled (composite) samples, with each pool consisting of 3 individual egg samples. Therefore, 2 pools were constituted with the 6 eggs available from 2004. Samples were analyzed for OCs and BFRs at the Great Lakes Institute for Environmental Research at the University of Windsor, Windsor, Ontario, Canada. Organochlorines and BFRs were analyzed using a gas chromatograph with a mass selective detector operated in the electron impact mode and using selected ion monitoring. More details are given in Braune et al. [13]. The nominal detection limit for OCs was 0.3 ng g1 wet weight, therefore in the same range as for samples from other colonies. For BFRs, the method limit of quantification was 0.01 ng g1 wet weight. Overall, detection limits and validation standards of both methods used in the present study for OC and BFR analyses were comparable.

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Determination of PFASs

In the present study, PFASs were not determined in Seymour Island. Analyses of PFASs (perfluorooctanoate [PFOA], perfluorononanoate [PFNA], and perfluorooctane sulfonate [PFOS]) were performed for Svalbard and Russian archipelagos by the Analytical Environmental Chemistry Unit at Stockholm University (Sweden) and were previously described in Miljeteig et al. [11]. Method detection limits were determined on the basis of 5 blank extraction experiments and ranged between 0.02 ng g1 and 0.5 ng g1 wet weight for the different analytes. Recovery rates of the stable isotope mass-labeled internal standards were, on average, 98% and 94% for 18O2-PFOS and 13 C4-PFOA, respectively. Greenland eggs were analyzed at the Laboratory of Environmental Toxicology in Oslo following the procedure described in Berger and Haukås [17]. Briefly, an 1100 series high-pressure quaternary gradient pump and auto-injector (Agilent Technologies) were coupled to a triple quad–MS/MS (API 3000 LC/MS/MS system). The injection volume was 10 mL. As for Svalbard and Russia samples, separation was achieved on a Discovery HS C18 column (Supelco). The target compounds were separated at a flow rate of 200 mL/min using 2 mM NH4OAc in both methanol and water. Method detection limits ranged between 0.1 ng g1 and 0.84 ng g1 wet weight for the different analytes. Recovery rates were, on average 94%, 95%, and 104% for PFOA, PFNA and PFOS, respectively. Determination of Hg

The analyses of Hg in eggs from Svalbard, Greenland, Franz Josef Land, and Severnaya Zemlya were performed by the National Veterinary Institute (Oslo, Norway). Homogenates were decomposed with a mixture of nitric acid and hydrogen peroxide using a closed system for microwave digestion. The amount of Hg in samples was determined using cold vapor atom absorption spectrophotometry (Varian SpectrAA 600; Varian). A quality control standard was used to control the standard curve. Certified reference materials and blank samples were analyzed with the samples in every run, and the reference materials used (TORT-2, LUTS-1, and DORM-2) were deemed acceptable compared with the certified values with 95% confidence intervals. Ivory gull eggs from Seymour Island were analyzed for total Hg at the National Wildlife Research Centre using an advanced mercury analyzer (AMA-254) equipped with an ASS-254 autosampler for solid samples according to Canadian Wildlife Service method MET-CHEM-AA-03E [18]. The method employs direct combustion of the sample in an oxygen-rich atmosphere. Analytical accuracy was determined using 4 standard reference materials (DOLT-2, DOLT-3, and TORT2, obtained from the Canadian National Research Council; Oyster Tissue 1566b, obtained from the US National Institute of Standards and Technology) and 15 random egg samples analyzed in replicate. Recovery of reference materials was within the confidence interval of the certified values and the nominal detection limit for total Hg was 0.05 mg g1 dry weight. Data treatment and statistical analyses

Several compounds that were detected or analyzed in less than 60% of the samples were excluded from statistical analyses, including p,p0 -dichlorodiphenyldichlorethane (p,p0 DDD), o,p0 -dichlorodiphenyltrichloroethane (o,p0 -DDT), BDE209, perfluorohexane sulfonate, endosulfan I, endosulfan II and endosulfan sulfate. Values below the quantification limit were

M. Lucia et al.

taken into account in calculation of the means and medians by assigning them values one-half of the detection limit for the given contaminant (e.g., a value 0.05) and was not significantly different between colonies (Kruskal–Wallis test, p > 0.05), contaminant concentrations are expressed in nanograms per gram wet weight. Moreover, this choice also allowed us to compare the present results with those of other studies of Arctic species. Because normality and homogeneity of variance were not achieved, despite log10(xþ1) transformation (Cochran C test), non-parametric analysis of variance (Kruskal–Wallis and Mann–Whitney U-test) was applied to assess differences in contaminant concentrations between colonies. Moreover, the Spearman test was applied to all correlations achieved in the present study. Principal component analysis was used to identify trends in the distribution of eggs collected from each colony in regards of their contaminant levels. Two principal component analyses were realized: 1 encompassing eggs from Seymour Island (Canada) and 1 excluding those eggs. The latter was therefore realized with OC (including S3CHB), BFR, and PFAS concentrations, whereas the first encompassed only OC (without S3CHB) and BFR values. Contaminants not measured and those under the detection limits in 1 or more colonies were not included in the analyses (e.g., cis-chlordane, dieldrin, PFOA). The PCBs and BDEs were encompassed in the principal component analyses as the sum of 12 PCB congeners (S12PCB) and the sum of 5 BDE congeners (S5BDE). Each contaminant concentration was first normalized (mean was subtracted and the difference was then divided by standard deviation). All analyses were performed using Statistica Ver 7.1 software. RESULTS

Contaminant concentrations in the eggs

The median concentrations of OCs and Hg are presented in Table 1, and BFR and PFAS concentrations are given in Table 2. The 12 PCB and 5 BDE congener concentrations given in both tables correspond to the common data available between colonies (i.e., contaminants measured and above detection limits for more than 60% of the samples analyzed). For some of the colonies, however, more PCB congeners were measured (up to 85 in Canadian eggs). Those results were not specified in the present study because of the aim to compare data between colonies. All PCB congeners were positively correlated with each other (R comprised between 0.29 and 0.97; Spearman test, p < 0.05), with the exception of PCB-52 and PCB-137. In the same way, all polybrominated diphenyl ether (PBDE) congeners were positively correlated, with R varying between 0.60 for BDE-28 and BDE-153 and 0.97 for BDE-47 and BDE-100. Mercury, however, was positively linked to trans-nonachlor (R ¼ 0.38), PCB-52 (R ¼ 0.32), and BDE-28 (R ¼ 0.43), whereas it was negatively correlated to b-hexachlorocyclohexane (b-HCH; R ¼ –0.31). The latter was also negatively correlated with all PBDEs except BDE-28 (R comprised between –0.34 and –0.39). Oxychlordane was significantly correlated with almost all of the other contaminants studied, with the exception of b-HCH, p,p’-DDT and PCB-52

Circumpolar contamination of the high-Arctic ivory gull

Environ Toxicol Chem 34, 2015 1

1

Table 1. Median and ranges (minimum–maximum) for organochlorine (ng g wet wt) and mercury (mg g homogenate samplesa Seymour Island

Station Nord

Svenskøya

1555

wet wt) concentrations analyzed in ivory gull egg

Nagurskoe

Cape Klyuv

Domashny

Median

Range

Median

Range

Median

Range

Median

Range

Median

Range

Median

Range

Lipid %

10.3

10.1–10.5

11.0

5.2–12.2

9.9

8.6–12.3

10.3

9.5–12.1

9.1

8.1–10.3

10.0

6.9–11.5

p,p0 -DDE p,p0 -DDT Oxychlordane Trans-nonachlor Cis-chlordane b-HCH Mirex Dieldrin HCB

1098 11.4 171 86.7 na 16.6 16.9 na 53.2

1034–1161 8.8–14.0 149–193 80.1–93.2 na 15.1–18.0 16.0–17.9 na 51.8–54.5

1450 6.3 116 96.5 2.9 8.8 33.8 50.3 70.8

483–3621 1.6–41.2 32.6–228 31.7–353 1.0–10.8 3.4–13.7 11.6–62.0 13.0–70.5 24.6–150

1328 22.7 156 67.1 21.2 10.6 30.1 na 55.1

933–3239 10.1–47.0 95.3–319 39.7–170 8.1–51.7 6.5–17.9 21.6–46.7 na 45.3–113

3177 40.9 310 107 na 16.7 49.6 61.9 97.4

1532–3864 32.4–45.7 130–413 75.6–527 na 10.4–30.6 28.3–67.7 51.7–171 79.2–112

1366 32.5 142 124 na 11.6 31.0 44.3 55.8

813–1915 20.9–69.5 98.9–188 26.5–175 na 8.9–31.5 21.0–43.2 21.3–59.3 41.0–90.9

984 21.2 104 29.7 na 28.3 19.5 23.1 59.8

341–7407 18.3–45.1 45.0–285 20.5–58.3 na 18.8–45.1 13.2–65.4 13.7–44.2 42.4–93.5

na na na na

na na na na

46.8 72.7 11.2 128

13.1–86.1 21.4–116 3.28–25.3 37.8–228

30.6 56.7 8.77 95.7

13.1–131 26.9–213 4.53–23.2 45.0–367

63.9 143.6 22.8 222.6

40.2–314 82.2–349 15.3–39.3 138–703

38.4 84.9 17.3 141

12.5–86.7 30.1–102 7.37–26.1 50.4–198

13.2 30.7 8.42 52.0

7.01–24.9 13.7–43.4 3.35–16.9 28.4–79.6

PCB-52 PCB-99 PCB-101 PCB-105 PCB-118 PCB-128 PCB-137 PCB-138 PCB-156 PCB-180 PCB-183 PCB-194 S12PCBc S3MO-PCBd

1.7 30.8 1.9 7.8 31.4 7.1 1.3 104 1.7 45.0 9.1 4.7 246 41.0

1.7–1.8 30.5–31.2 1.3–2.4 7.2–8.5 29.6–33.2 7.0–7.2 1.2–1.5 102–105 1.6–1.8 44.8–45.3 8.9–9.3 4.5–4.9 244–248 38.4–43.6

9.4 176 4.2 33.7 124 36.8 23.5 420 21.9 333 64.9 36.3 1284 181

2.0–15.5 50.1–373 1.0–16.2 9.3–53.9 38.4–227 11.2–85.7 7.6–52.0 132–920 6.9–32.7 107–656 21.0–139 12.7–64.5 399–1996 54.6–313

6.4 151 9.4 31.6 125 25.6 31.3 522 26.8 310 57.9 34.8 1363 184

2.3–9.5 99.2–346 4.5–17.9 21.9–57.4 89.1–188 13.2–79.9 18.9–57.3 312–1029 19.4–43.7 217–588 39.0–101 29.1–60.1 881–2557 131–281

12.0 390 15.3 61.5 213 107 70.5 986 42.9 536 112 65.0 2658 317

6.1–25.6 173–503 9.8–35.1 36.9–116 134–381 45.6–119 30.5–90.6 448–1186 21.6–60.2 267–800 61.8–162 32.6–101 1276–3389 193–555

4.5 191 8.7 35.7 125 44.9 36.4 491 22.1 306 62.3 37.1 1359 189

2.5–36.2 120–260 5.2–31.1 20.5–40.4 74.7–145 21.3–70.6 24.6–45.3 302–662 14.3–30.7 180–379 41.0–81.6 19.8–57.6 825–1772 110–216

2.5 137 4.8 28.2 97.7 28.3 24.8 303 15.1 139 35.4 13.9 823 141

1.5–10.4 67.2–584 3.2–17.6 13.5–60.0 42.8–326 8.6–131 12.3–116 148–1282 7.5–36.1 78.2–557 19.6–163 8.7–43.5 420–3318 63.9–422

Hg

1.1

0.40–3.9

0.24

0.12–0.84

0.14

0.08–0.24

0.23

0.08–0.24

0.20

0.16–0.48

0.11

0.06–0.30

CHB-26 CHB-50 CHB-62 S3CHBb

a Samples are from the Seymour Island (Canada; n ¼ 2, except for Hg n ¼ 6) colony [12,13]; the Station Nord colony (Greenland; n ¼ 10); the Svenskøya colony (Svalbard, Norway; n ¼ 10); and the Nagurskoe (n ¼ 6), Cape Klyuv (n ¼ 7), and Domashny (n ¼ 12) colonies (Russian Arctic) [11]. b Sum of the toxaphene congeners, CHB-26, CHB-50, and CHB-62. c Sum of PCB-52, PCB-99, PCB-101, PCB-105, PCB-118, PCB-128, PCB-137, PCB-138, PCB-156, PCB-180, PCB-183, PCB-194. d Sum of mono-ortho (MO) PCB-105, PCB-118, and PCB-156. Hg ¼ mercury; na ¼ not analyzed; DDE ¼ dichlorodiphenyldichloroethylene; DDT ¼ dichlorodiphenyltrichloroethane; b-HCH ¼ b-hexachlorocyclohexane; HCB ¼ hexachlorobenzene; CHB ¼ chlorobornanes; PCB ¼ polychlorobiphenyl.

The sum of 12 PCB congener medians in eggs of ivory gulls ranged between 246 ng g1 wet weight in Seymour Island, Canada, and 2658 ng g1 wet weight in Nagurskoe, Russia (Table 1). The congeners accounting for more than 10% of the

(R comprised between 0.29 and 0.82). The same result was also observed for mirex, which was positively correlated with all the contaminants except b-HCH and p,p’-DDT (R comprised between 0.41 and 0.97).

Table 2. Median and ranges (minimum–maximum) for brominated flame retardant and perfluorinated alkyl substance (ng g1 wet wt) concentrations analyzed in ivory gull egg homogenate samplesa Seymour Island

Station Nord

Svenskøya

Nagurskoe

Cape Klyuv

Domashny

Median

Range

Median

Range

Median

Range

Median

Range

Median

Range

Median

Range

BDE-28 BDE-47 BDE-99 BDE-100 BDE-153 S5BDE HBCD

0.30 2.81 0.45 0.27 0.08 3.91 0.22

0.16–0.44 2.45–3.16 0.42–0.48 0.26–0.28 0.08–0.09 3.67–4.14 0.18–0.26

0.12 9.37 3.08 1.01 1.60 15.6 7.84

0.04–0.23 2.48–17.4 0.72–5.90 0.28–2.14 0.49–2.46 4.01–26.5 1.49–14.8

0.10 7.98 1.72 1.14 1.31 11.8 7.52

0.05–0.22 5.66–13.9 1.09–3.15 0.60–1.53 0.77–2.01 8.21–20.6 3.81–12.9

0.26 19.2 3.17 1.73 2.01 26.6 14.1

0.16–0.56 9.47–43.6 2.38–5.54 0.99–3.46 1.17–2.62 14.5–55.3 7.19–28.4

0.25 17.0 2.76 1.37 1.28 23.5 11.7

0.06–0.38 4.72–24.9 0.92–3.39 0.31–2.37 0.56–1.84 6.57–32.9 4.40–14.0

0.05 2.33 0.52 0.26 0.34 3.97 3.85

0.02–0.10 1.26–4.83 0.33–1.02 0.16–0.50 0.19–1.27 2.10–6.08 1.42–11.9

PFOA PFNA PFOS S3PFAS

na na na na

na na na na

1.33 4.89 25.8 32.6

0.98–1.89 3.32–6.47 10.9–60.8 18.8–66.2

nd 1.04 79.2 79.5

nd 0.40–2.70 24.2–113 23.6–115

0.30 1.34 59.1 60.8

nd–0.40 0.77–1.48 25.2–89.9 26.3–91.8

0.23 0.99 66.1 67.4

nd–0.31 0.65–1.21 20.9–97.3 21.8–98.6

0.22 1.49 57.7 59.2

nd–0.37 0.83–2.15 17.7–117 18.6–118

From the Seymour Island colony (Canada; n ¼ 2) [13]; the Station Nord colony (Greenland; n ¼ 10); the Svenskøya colony (Svalbard, Norway; n ¼ 10); and the Nagurskoe (n ¼ 6), Cape Klyuv (n ¼ 7), and Domashny (n ¼ 12) colonies (Russian Arctic) [11]. na ¼ not analyzed; nd ¼ below detection limit; BDE ¼ brominated diphenyl ether; HBCD ¼ hexabromocyclododecane; PFOA ¼ perfluorooctanoate; PFNA ¼ perfluorononanoate; PFOS ¼ perfluorooctane sulfonate; PFAS ¼ perfluorinated alkyl substance. a

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S12PCB were PCB-138, PCB-180, PCB-99, and PCB-118, with an average of 36%, 22%, 14%, and 10%, respectively. Among OC compounds, p,p’-DDE median concentrations ranged from 984 ng g1 in Domashny to 3177 ng g1 in Nagurskoe (Table 1). The sum of BDE median concentrations ranged between 3.9 ng g1 in Seymour Island and 26.6 in Nagurskoe (Table 2). The main congeners are BDE-47 and BDE-99, with a percentage contributions of 67% and 15% of the sum BDEs, respectively. In the present study, PFOS was the most prominent PFAS and represented 94% of the PFAS load in ivory gulls (Table 2). Median concentrations of PFOS ranged between 25.5 ng g1 in Station Nord and 79.2 ng g1 in Svenskøya. In contrast, the PFNA median concentration of Station Nord was significantly higher than in other colonies, at 4.89 ng g1 (Kruskal–Wallis test, p < 0.05). Concentrations of PFOA in ivory gulls from Greenland also were significantly higher than Russian colonies (Kruskal–Wallis test, p < 0.05; Table 2). Moreover, the only positive correlation observed was between PFNA and PFOA (R ¼ 0.75; Spearman test, p < 0.05). Finally, Hg concentrations were significantly higher in Seymour Island, Canada, compared with the other colonies (Kruskal–Wallis test, p < 0.05; Figure 2). Differences of contaminant levels between colonies

Figure 3 presents a principal component analysis that was performed on ivory gull data from Seymour Island, Station Nord, Svenskøya, Nagurskoe, Cape Klyuv, and Domashny Island to identify trends in the distribution of OCs, BFRs, and Hg between colonies. Perfluorinated alkyl substances were not taken into account in this analysis because of the lack of data from Seymour Island. The first 2 axes extracted 65.4% of the variance of the data clouds. The first axis (PC1) was negatively correlated with most of the OCs and BFRs, whereas the second axis (PC2) was negatively correlated with b-HCH concentrations (Figure 3A). The projection of the egg samples (Figure 3B) demonstrated that ivory gulls from Nagurskoe were characterized by higher PCBs and PBDEs concentrations, whereas gulls from Domashny by lower contaminant levels. In contrast, gulls from Seymour Island were discriminated by higher Hg concentrations. Figure 4 depicts the distribution of ivory gull coordinates on the principal component analysis first axis (PC1; Figure 3)

Hg concentration (µ g g-1 wet wt)

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Figure 2. Mean mercury (Hg) concentrations (mg g wet wt  standard deviation) in ivory gull eggs form Seymour Island (SE; Canada), Station Nord (SN; Greenland), Svenskøya (SV; Svalbard, Norway), Nagurskoe (NA; Franz Josef Land, Russia), Cape Klyuv (KL; Franz Josef Land, Russian Arctic), and Domashny Island (DO; Severnaya Zemlya, Russian Artic). Significant differences between colonies at the level a ¼ 0.05 (Mann–Whitney test) are indicated by letters.

according to the different longitudes of the 6 colonies studied. Negative coordinates on PC1 corresponded to higher OC and BFR concentrations. Contaminant concentrations were higher in Nagurskoe (longitude: 478370 E) and lower both west (Seymour Island, longitude: 1018160 W) and east (Domashny, longitude: 918050 E) of it. Another principal component analysis was realized encompassing the PFAS (PFNA, PFOS) and S3CHB results and therefore without the Seymour Island data (Figure 5). Perfluorononanoate values were not included in this analysis because of the percentage of data below the quantification limit. Figure 5 encompasses the projection of each sample and variable on the first and second axes, which extracted 59.6% of the variance of the data clouds. Thus, this projection allowed dissociating the trends in PFAS concentrations between colonies. The first axis (PC1) was correlated with most of the OCs and BFRs whereas the second axis (PC2) was positively associated with b-HCH and PFOS concentrations and negatively with PFNA and Hg (Figure 5A). Principal component analysis results demonstrated that ivory gulls from Station Nord were characterized by higher PFNA concentrations but lower PFOS levels (Figure 5B). The second axis coordinates were projected against colony longitudes (Figure 6). This graphic clearly revealed the lower PFOS concentrations in ivory gull eggs sampled in Station Nord. DISCUSSION

Contaminant concentrations in eggs and toxicity significance

Previous studies have described the high contaminant concentrations reached in the ivory gull, a species characterized by its high-Arctic range [11,19]. The present study, however, for the first time encompasses and compares data in eggs from most of the breeding range of this seabird species through the circumpolar Arctic. Polychlorobiphenyls reached elevated concentrations in eggs of ivory gulls with the sum of 12 congeners reaching 2658 ng g1 wet weight in Nagurskoe, Russia (Table 1). A previous review [20] noted that studies in which congener-specific analyses were performed on eggs demonstrated the highest concentration presence of the di-ortho PCB 138, as observed in the present study. Some studies also reported differences in the PCB 156/105 ratio range between avian species originating from Europe and North America. North American biota often demonstrated a PCB 156/105 ratio range of 0.3 to 0.5, whereas birds from Europe, especially the Netherlands, had a ratio range between 1 and 1.5 [20–22]. In the present study, Canadian eggs displayed a lower PCB 156/105 ratio, averaging 0.2, compared with European ivory gull, whose ratios ranged from 0.5 in Domashny, Severnaya Zemlya, to 0.8 in Svenskøya, Svalbard. Although high levels were reached, especially in Nagurskoe, Franz Josef Land, these results were below the lowest-observed-effect level (LOEL) range (3.5–22 mg SPCBs g1 wet wt) in eggs for various endpoints of reproductive success (egg mortality, deformities, hatching success, and parental attentiveness) [20,23]. In ivory gulls, SPCB concentrations ranged between 0.3 mg g1 and 2.7 mg g1 wet weight depending on the colony, therefore below LOEL levels found for reproductive effects. When more PCB congeners were taken into account in a previous study, however, concentrations from Nagurskoe eggs were above this LOEL level [11]. Indeed, that study encompassed 28 congeners and demonstrated a mean concentration in Nagurskoe of 4.5 mg g1 wet weight (expressed in lipid weight in the study) [11]. However, it is unlikely that egg concentrations would continue to

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PC1 (50.68% of total variation) Figure 3. Principal component analysis based on the organochlorines (OCs), brominated flame retardants (BFRs), and mercury (Hg) concentrations in the eggs of ivory gulls from Seymour Island (SE; Canada), Station Nord (SN; Greenland), Svenskøya (SV; Svalbard, Norway), Nagurskoe (NA; Franz Josef Land, Russia), Cape Klyuv (KL; Franz Josef Land, Russian Arctic), and Domashny Island (DO; Severnaya Zemlya, Russian Artic). (A) Variable projections in the first 2 dimensions (principal components 1 [PC1] and 2 [PC2]) and (B) individual projections. Relative weight of the variance of each component is indicated as a percentage. BDE ¼ brominated diphenyl ether; p,p0 -DDE ¼ dichlorodiphenyldichloroethylene; p,p0 -DDT ¼ dichlorodiphenyldichloroethane; HCB ¼ hexachlorobenzene; PCB ¼ polychlorobiphenyl; HBCD ¼ hexabromocyclododecane; b-HCH ¼ b-hexachlorocyclohexane.

increase if more congeners were added, because most of the congeners accounting for total PCB concentration were included in both the present study and the previous study [11]. Several review papers mentioned a no-observed-effect level (NOEL) range for SPCB of 1.3 mg g1 to 11.0 mg g1 wet weight for effects related to reproductive success in seabirds [20,23]. Most of the eggs from Nagurskoe (4 out of 6) were above the NOEL for hatching success in Foster terns (Sterna forsteri), suggesting that such effects could be observed [20]. In parallel, p,p’-DDE was also found in high concentrations, especially in Nagurskoe, where 67% of the eggs exceeded the threshold level of 3000 ng g1 wet weight, known to disrupt the

reproductive success of the brown pelican (Pelecanus occidentalis) and the bald eagle [24,25]. Although PCB and p,p0 DDE concentrations could be of toxicological concern and warrant monitoring, the majority of the OCs displayed concentrations below toxicity threshold levels. Polybrominated diphenyl ethers constitute one of the main classes of brominated compounds used as flame retardant additives [26]. These compounds are ubiquitous in the environment and have been detected in most ecosystems and taxa, along with several unregulated halogenated contaminants [27]. The sum BDE concentrations ranged between 3.9 ng g1 in Seymour Island and 26.6 ng g1 in Nagurskoe. Potential

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3 PC1 coordinate

exposure-related effects included disruption of reproductive hormone levels [28], competitive interactions with thyroid hormone carrier proteins [29], and modification of egg composition [30]. More recently, a study also demonstrated that bone metabolism and mineral composition of ring-billed gulls (Larus delawarensis) breeding in a highly urbanized area in Canada may be impacted by flame retardants [31]. However, it is difficult to draw conclusions on the potential effects of flame retardants on ivory gulls. This species potentially either could be impacted by these contaminants or could be less sensitive than other species. Overall, the lack of studies to evaluate effects of these compounds makes it difficult to assess the toxicity of flame retardants on ivory gulls. Recent environmental studies have demonstrated the widespread occurrence of PFASs in tissues of biota from the Arctic [7]. One of the most ubiquitous PFASs of concern in arctic biota is PFOS [32]. In the present study, PFOS was indeed the most prominent PFAS. Unfortunately, effects of these compounds are poorly known and unclear. Perfluorooctane

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Figure 4. Distribution of ivory gull coordinates on the principal component analysis first axis (PC1; Figure 3) according to the different longitudes of the 6 colonies from which eggs were sampled: Seymour Island (SE; Canada), Station Nord (SN; Greenland), Svenskøya (SV; Svalbard, Norway), Nagurskoe (NA; Franz Josef Land, Russia), Cape Klyuv (KL; Franz Josef Land, Russian Arctic), and Domashny Island (DO; Severnaya Zemlya, Russian Artic). Western longitudes have negative coordinates, whereas eastern longitudes have positive ones.

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Figure 5. Principal component analysis based on the perfluorinated alkyl substances (PFASs), perfluorononanoate (PFNA), perfluorooctane sulfonate (PFOS), organochlorines (OCs), brominated flame retardants (BFRs), and mercury (Hg) concentrations in the eggs of ivory gulls from Station Nord (SN; Greenland), Svenskøya (SV; Svalbard, Norway), Nagurskoe (NA; Franz Josef Land, Russia), Cape Klyuv (KL; Franz Josef Land, Russian Arctic), and Domashny Island (DO; Severnaya Zemlya, Russian Artic). (A) Variable projections in the first 2 dimensions(principal components 1 [PC1] and 2 [PC2]) and (B) individual projections. Relative weight of the variance of each component was indicated as a percentage. BDE ¼ brominated diphenyl ether; p,p0 -DDE ¼ dichlorodiphenyldichloroethylene; p,p0 -DDT ¼ dichlorodiphenyldichloroethane; HCB ¼ hexachlorobenzene; PCB ¼ polychlorobiphenyl; HBCD ¼ hexabromocyclododecane; b-HCH ¼ b-hexachlorocyclohexane; CHB ¼ chlorobornanes; PFOS ¼ perfluorooctane sulfonate; PFNA ¼ perfluorononanoate.

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Figure 6. Distribution of ivory gull coordinates on the principal component second axis (PC2; Figure 5) according to the different longitudes of 5 colonies: Station Nord (SN; Greenland), Svenskøya (SV; Svalbard, Norway), Nagurskoe (NA; Franz Josef Land, Russia), Cape Klyuv (KL; Franz Josef Land, Russian Arctic), and Domashny Island (DO; Severnaya Zemlya, Russian Artic). Western longitudes have negative coordinates, whereas eastern longitudes have positive coordinates.

sulfonate is known to have a high affinity to the protein albumin, which may trigger a competitive interaction between PFOS and T4 for binding sites on albumin. This compound could therefore easily trigger changes in hormone homeostasis [33]. Levels recorded in the present study were below those reported in glaucous gulls from the Norwegian Arctic [34]. These authors suggested that PFOS alone would not contribute to altering the circulating hormone status and cause adverse effects on glaucous gulls. Nevertheless, because data are scarce, potential sublethal effects could not be ruled out entirely. Based on a review of the literature, it has been suggested that Hg concentrations of 0.5 mg g1 to 2.0 mg g1 wet weight in eggs are sufficient to alter reproductive success in a variety of bird species [35]. Concentrations in the majority of eggs from Seymour Island exceeded these threshold values, whereas only 1 egg in Station Nord was above 0.5 mg g1 wet weight. Mercury does not represent a threat for the survival of the species but could trigger reproductive impairments and sublethal effects in the ivory gull from Seymour Island, as previously reported [12]. Overall, the levels of OCs, BFRs, and PFASs did not suggest direct lethal exposure to these compounds. Their potential synergetic or additive sublethal effects, however, warrant continued monitoring. Spatial variation in contaminant levels

The projection of the egg samples (Figure 3) demonstrated that ivory gulls from Nagurskoe were characterized by higher PCB and PBDE concentrations, whereas gulls from Domashny were characterized by lower contaminant levels. On the other hand, gulls from Seymour Island were distinguished by higher Hg concentrations. Indeed, mean Hg concentrations were significantly higher in Canada compared with those in other colonies. Previous reports from studies examining the Arctic have shown an east–west increase of Hg concentrations in marine species [36]. This trend was verified in the ivory gull in the present study. These higher Hg levels in biota may be related in part to naturally higher Hg concentrations in Canadian Arctic sediments [36]. However, recent studies have suggested that Asian air masses are depositing large amounts of anthropogenic Hg from China into the Canadian Arctic [37]. The steady increase of Hg concentrations noticed in ivory gull and other seabird eggs in recent decades could therefore be related in part to increased emissions from Asia [12].

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The results tend to highlight a bidirectional gradient in OC and BFR concentrations, peaking in Nagurskoe (longitude: 478370 E) and decreasing to both the western (Seymour Island, longitude: 1018160 W) and eastern (Domashny, longitude: 918050 E) edges of the species breeding range. Ivory gulls from Domashny Island displayed OC and BFR concentrations more aligned with the Seymour Island results. These regional differences, especially between Russian colonies, may be linked both to the existence of local sources of contamination and to differences in local food web compositions. The ivory gull is an opportunistic feeder that may well adapt to local feeding conditions and therefore prey on items with differential contamination levels. Moreover, Domashny is situated farther away from the potential inflow of contaminants from the Gulf Stream and the West Atlantic than Nagurskoe. Perfluorinated alkyl substances demonstrated divergent patterns depending on the compound considered. For PFNA, a clear gradient of exposure, ranging from a low in Cape Klyuv, Franz Josef Land to a much higher level in Station Nord, Greenland, can be observed. Variance analyses also highlighted higher PFOA concentrations in ivory gulls from Greenland compared with Russian colonies. In contrast, PFOS seemed to demonstrate a completely opposite tendency, with lower levels in Station Nord, Greenland. This result contrasted with previous observation in Arctic species from Greenland. Indeed, polar bears from south Hudson Bay and Greenland had significantly greater PFOS concentrations than in Svalbard, the High Arctic, and the Northwest Territory [38]. Perfluorinated alkyl substances are used in several chemical products such as stain repellents, cleaners, fire-fighting foams, and lubricants. These compounds persist in the environment and are transported worldwide, even to the remote Arctic region. Two pathways to the Arctic have been identified: atmospheric transport of precursors and direct long-range transport via ocean currents [7]. The contribution of each pathway to the transport of these substances to the Arctic remains unclear. Different concentrations in different regions are likely due to different transport pathways of PFASs along the distribution of the ivory gulls. For example, concentrations of some PFASs, such as PFOA and PFOS, recently demonstrated decreasing trends in ringed seals and polar bears from Greenland [39]. This decreasing trend appeared, however, at a later time than in seals and polar bears from Canada. Overall, egg samples in the present study were collected between 2004 for Canada and 2010 for Greenland. Although the time gap between collections is limited, especially between the Norwegian and Russian colonies, which were sampled only 1 yr apart, spatial variations observed could be influenced partly by divergent temporal trends between colonies. The differential transport pathways of contaminants to various locations in the Arctic may trigger a faster or slower response in the colonies considered. For example, different temporal trends of b-HCH concentrations were observed in biota from the Canadian Arctic, with unchanged or increasing concentrations, and in Greenland, with decreasing concentrations observed in ringed seals [40]. These different temporal trends are potentially linked to b-HCH that enters the western Arctic via ocean currents passing through the Bering Strait and then is transported eastward in the Beaufort Sea through the Canadian archipelago [40]. Increasing Hg concentrations linked with increasing fluxes to the Arctic were also observed in Canadian Arctic species over the past few decades, although time series data have shown no change or decreasing patterns in seabirds at lower latitudes [41]. Consequently, further investigations should consider sampling

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eggs from the same year to have a full representation of spatial trends in the breeding distribution of the species. The present study’s results highlight the divergent trends depending on the considered contaminant. Organochlorines and BFRs seemed to display the same geographical pattern, whereas PFASs trends differed according to the type of compound. Overall, species living in the same environments and geographical locations displayed differential spatial trends. These divergent patterns between species demonstrate that exposure to pollutants is related not only to chemical properties of the considered element and its presence in an ecosystem but also to the intrinsic biology and ecology of a particular species. Finally, it is noteworthy that different concentrations were observed in breeding colonies potentially using the same wintering grounds or alternating wintering grounds between years [9]. Therefore, differences in contaminant loads observed between colonies may be the result of the contaminant exposure on the breeding location of gulls. Further studies should investigate more thoroughly the foraging behavior and range of this species to develop a better picture of the potential contamination sources. Increasing the sample size would also be interesting to better investigate contamination variations in a species with a complicated spatial and temporal population structure. CONCLUSION

The most quantitatively abundant OCs found in the ivory gull eggs were p,p0 -DDE and SPCB. Most of the PCB and PBDE congeners were positively intercorrelated. Mercury concentrations were higher in Seymour Island, Canada, compared with the other 5 colonies. Multivariate analyses demonstrated that eggs from Nagurskoe often were characterized by higher OC and BFR concentrations, whereas eggs from Seymour Island, especially Domashny, displayed lower levels. These results demonstrate an increase in OC and BFR concentrations between Seymour Island and Nagurskoe, followed by a gradual decrease in colonies located east of the latter. In contrast, PFAS concentrations, especially PFOA and PFNA, were higher in Station Nord, Greenland. Overall, the present study highlighted divergent spatial patterns according to the class of contaminant considered. Some of the contaminants, especially PCBs and p,p0 -DDE, exceeded threshold levels known to disrupt the reproductive success of avian species. The levels of OCs, BFRs, and PFASs did not suggest direct lethal exposure to these compounds, but their potential synergetic or additive sublethal effects warrant continued monitoring. Acknowledgment—The authors thank the European Commission for its financial support through a Marie Curie fellowship to M. Lucia and the Danish Environmental Protection Agency for funding D. Boertmann to collect the Greenland eggs (grant no. MST-112-00268). This project was part of the work plan of the Joint Norwegian–Russian Commission on Environmental Protection. M. Gavrilo thanks her colleagues A. Volkov and E. Volkova, a field crew led by O. Prodan, and a Vorkuta helicopter crew commanded by S. Kiryushkin. Data availability—All data, associated metadata, and calculation tools are available on request from the authors ([email protected], [email protected]). REFERENCES 1. Serreze MC, Holland MM, Stroeve J. 2007. Perspectives on the Arctic’s shrinking sea-ice cover. Science 315:1533–1536. 2. Boonstra R. 2004. Coping with changing northern environments: The role of the stress axis in birds and mammals. Integr Comp Biol 44:95– 108.

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