Trends of Perfluorinated Alkyl Substances in Herring Gull Eggs from

Sep 7, 2007 - The present study reports on concentrations, patterns, and temporal trends (1983, 1993, and 2003) of 16 perfluorinated alkyl substances ...
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Environ. Sci. Technol. 2007, 41, 6671-6677

Trends of Perfluorinated Alkyl Substances in Herring Gull Eggs from Two Coastal Colonies in Northern Norway: 1983-2003 JONATHAN VERREAULT,† U R S B E R G E R , * ,‡,§ A N D GEIR W. GABRIELSEN† Norwegian Polar Institute, Tromsø, NO-9296, Norway, Department of Applied Environmental Science, Stockholm University, Stockholm, SE-106 91, Sweden, Norwegian Institute for Air Research, Tromsø, NO-9296, Norway

The present study reports on concentrations, patterns, and temporal trends (1983, 1993, and 2003) of 16 perfluorinated alkyl substances (PFAS) in whole eggs of herring gulls (Larus argentatus) from two geographically isolated colonies in northern Norway. Perfluorooctane sulfonate (PFOS) was the predominant PFAS in all eggs with mean concentrations up to 42 ng/g wet weight (ww) in samples from 2003. Perfluorohexane sulfonate (PFHxS) and perfluorodecane sulfonate (PFDcS) were found at concentrations several orders of magnitude lower than PFOS. The general accumulation profile of perfluorocarboxylates (PFCAs) in herring gull eggs was characterized by high proportions of odd and long carbon (C) chain length compounds in which perfluoroundecanoate (C11) and perfluorotridecanoate (C13) dominated with mean concentrations up to 4.2 and 2.8 ng/g ww, respectively. In both colonies PFOS concentrations in eggs showed a nearly 2-fold significant increase from 1983 to 1993, followed by a leveling off up to 2003. A comparable trend was found for PFHxS, whereas PFDcS was found to increase also between 1993 and 2003. PFCA concentrations showed marked significant increases during 1983-1993 associated with either a weak rise post-1993 (C8- to C11-PFCAs), although nonsignificant, or leveling off (C12- and C13-PFCAs). However, the composition of individual PFCAs (C8 to C15) to the summed concentrations of those eight PFCAs highly differed between the colonies and sampling years investigated. Present results suggest that direct and indirect local- and/ or remote-sourced inputs (atmospheric and waterborne) of PFCAs have changed over the last two decades in these two coastal areas of Northern Norway.

Introduction Perfluorinated alkyl substances (PFAS) have received growing scientific and regulatory interest over the past few years as a consequence of their ubiquitous detection in human and environmental samples, and potential impacts on human and wildlife health. PFAS-related chemicals have been used as surface-active agents in a multitude of manufactured and consumer products. Specifically, in North America and * Corresponding author phone: +46 8 674 7099; fax: +46 8 674 7637; e-mail address: [email protected]. † Norwegian Polar Institute. ‡ Stockholm University. § Norwegian Institute for Air Research. 10.1021/es070723j CCC: $37.00 Published on Web 09/07/2007

 2007 American Chemical Society

countries of the European Union (EU), uses of PFAS have primarily been in fire-fighting foams and impregnation agents for carpets, papers, and textiles. Currently available production figures for perfluorooctane sulfonate (PFOS), the most widely detected PFAS in environmental samples, suggest that the suspension in the manufacture of this chemical by the 3M company in 2000-2002 has led to a gradual decrease in its production and use within the EU for most of these applications (1). PFOS, which is listed as chemical for priority action, was recently accepted as fulfilling the criteria for classification as a persistent, bioaccumulative and toxic (PBT) substance (1) and persistent organic pollutant (POP) under the Stockholm Convention (2). A recent EU directive restricts the use of PFOS and PFOS-related compounds from June 27, 2008 in the EU member states, and concludes that perfluorooctanoate (PFOA) is suspected to have a similar risk profile to PFOS (3). Comprehensive sampling campaigns have ascertained that PFAS have an ubiquitous presence in the European environment (4) which also includes wildlife species occupying all trophic positions in the remote (European) Arctic marine food web (i.e., amphipods, fish, seabirds, and polar bears (Ursus maritimus)) (5-7). There is currently a large monitoring database of PFAS residues in wildlife that has shown that the compositional patterns in tissue/blood vary greatly among species and geographical locations, which suggests multiple discharge and emission sources (8). However, concentrations of PFAS that are of most environmental concern (mainly PFOS) in biota samples archived as far back as the 1960s have also been shown to fluctuate significantly over time. To date, temporal trend studies of PFOS in wildlife from northern Europe have been carried out in eggs of common guillemots (Uria aalge) (9) and liver of white-tailed sea eagles (Haliaeetus albicilla) (10) from the Baltic Sea, as well as in liver of Atlantic cod (Gadus morua) from the North Sea (4). These studies have shown that despite large interyear variations, a general tendency for increasing PFOS concentrations was observed in samples from the late 1960s and up to early 2000. Comparable PFOS and perfluorocarboxylate (PFCA) concentration variations over the last decades were also reported for Arctic marine mammal samples in North America and Greenland: e.g., ringed seals (Phoca hispida) (11, 12) and polar bears (13). In the present study, we investigated the parts-per-trillion (pg/g) concentrations and compositional patterns of 16 major PFAS comprised mainly of perfluorosulfonates (PFSs) and PFCAs, in whole eggs of herring gulls (Larus argentatus) from two geographically isolated colonies along the coast of Northern Norway. These colonies encompassed the southern and northern distribution range of herring gulls breeding in Northern Norway. Furthermore, a 3-point temporal trend of PFAS concentrations was examined in herring gull eggs collected in 1983, 1993, and 2003 for these colonies. The herring gull, a widespread colonial seabird species in Norway having a limited annual feeding range, is primarily a fishfeeder, although it may also feed opportunistically on crustaceans, seabird chicks, eggs, and terrestrial food sources (e.g., human refuse) (14). In the context of contaminant monitoring, herring gulls, and particularly their eggs, have been identified as key sentinel species of freshwater basin contamination in the densely populated and industrialized North American Great Lakes (15-17). In Norway, herring gull eggs also have proved to be advantageous for monitoring local brominated and chlorinated contaminant exposure in the marine environment (18-20). VOL. 41, NO. 19, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Experimental Section Sampling. A total of 30 freshly laid eggs of herring gulls were collected randomly from three major nesting sites along the coast of Northern Norway (Hornøya, Røst, and Hekkingen) in 1983, 1993, and 2003. Hornøya is located in the northeasternmost part of Northern Norway, whereas Røst and Hekkingen (both colonies hereafter referred to as Røst due to their proximity) are situated in the southern part along the west coast approximately 850 km from Hornøya (Figure S1, Supporting Information). Due to the important distance separating Hornøya and Røst, and the fact that herring gulls generally obtain their food locally with limited seasonal movements (14), these colonies were assumed to represent distinct population exposure scenarios. Details on the study area can be found in Knudsen et al. (20). Eggs were archived at the Tromsø University Museum (Tromsø, Norway) and kept frozen (-20 °C or below) until laboratory analyses, which were carried out in 2006. PFCAs and PFSs have environmental half-lives of several decades, and are therefore not expected to degrade during storage at -20 °C. Perfluorooctane sulfonamide (PFOSA) could possibly degrade to both PFOS and PFOA. However, as the concentration ratios found between PFOS and PFOSA as well as between PFOA and PFOSA showed no trend with sampling years, it could be concluded that no relevant transformation of PFOSA occurred during storage. Chemicals. The abbreviations of target analytes and origin of analytical standard compounds including the internal (surrogate) standard (IS) and recovery internal (volume) standard (RIS) are given in Table S1 in the Supporting Information. Solvents and reagents used were of highest commercial purity and employed as received. Water obtained from a Milli-Q water purification unit (Millipore AB, Solna, Sweden) was used. Sample Preparation. A 1 g aliquot of homogenized whole herring gull egg sample was transferred to a 13 mL polypropylene (PP)-centrifuge tube, and spiked with 2.5 ng of the IS 1,2,3,4-13C4-perfluoro-n-octanoic acid (13C4-PFOA; 50 µL of 50 pg/µL in methanol). The egg homogenate was then added 5 mL of acetonitrile, vortex mixed, extracted in an ultrasonic bath (15 min, room temperature) and centrifuged (5 min, 2000 rpm). The supernatant was transferred to a new PPtube, and the extraction was repeated with another 5 mL of acetonitrile. The combined extracts were concentrated to 1 mL under nitrogen. The concentrated extract underwent dispersive cleanup by vortex mixing (20 s) on 25 mg graphitized carbon (Supelclean ENVI-Carb 120/400, Supelco, Sigma-Aldrich, Stockholm, Sweden) and 50 µL glacial acetic acid in a 1.7 mL Eppendorf centrifuge tube. After centrifugation (10 min, 10 000 rpm), 0.5 mL of the cleaned-up extract was added 0.5 mL of 4 mM aqueous ammonium acetate, which led to the formation of a precipitate. The solution was vortex mixed and centrifuged again before the clear supernatant was transferred to an autoinjector vial for instrumental analysis, and 2.5 ng of the RIS 7H-perfluoroheptanoic acid (7H-PFHpA; 50 µL of 50 pg/µL in methanol) was added. Instrumental Analysis. PFSs including perfluorooctane sulfonamide (PFOSA) and 6:2 fluorotelomer sulfonate (6:2 FTS) were quantified using high performance liquid chromatography (HPLC) coupled to quadrupole-time-of-flight high-resolution mass spectrometry (Q-ToF-HRMS). ToFHRMS was preferred to tandem MS due to the lower detection limits as describe in Berger et al. (21). An Acquity Ultra Performance HPLC system (Waters, Milford, MA) was employed to inject aliquots of 20 µL extract onto an Ace 3 C18 reversed phase column (150 × 2.1 mm, 3 µm particles, Advanced Chromatography Technologies, Aberdeen, Scotland). The target compounds were separated at a flow rate of 200 µL/min using 4 mM NH4OAc in both methanol (A) 6672

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and water (B). The following binary gradient was applied: 0-0.5 min, 40% of A; 0.5-8 min, linear change to 95% of A; 8-18 min, 95% of A. The Premier Q-ToF-HRMS instrument (Micromass, Manchester, England) was employed in negative ion electrospray ionization (ESI(-)) mode. Mass spectra were registered in full scan mode (mass range m/z 150-720). The following optimized parameters were applied: Capillary voltage, 0.1 kV; sample cone voltage, alternating 25/50 V; desolvation temperature, 225 °C; source temperature, 90 °C; nitrogen desolvation gas flow, 800 L/h. Quantitative analysis was performed employing extracted mass chromatograms from full scan recording using the cone voltages and m/z (typical mass tolerance of 0.05 u) for the different analytes listed in Table S1 in the Supporting Information. For quantification of PFCAs, an Alliance 2695 HPLC system (Waters; degasser replaced with helium degassing) coupled to a Quattro II triple quadrupole MS (Micromass) was applied. Aliquots of 50 µL extract were injected onto a Discovery HS C18 column (50 × 2.1 mm, 3 µm particles, Supelco) and compound separation was achieved with the same binary gradient as described for PFSs. ESI(-) was used for ionization, and the MS instrument was employed in the multiple reaction monitoring (MRM) mode based on precursor-product ion combinations given in Table S1 in the Supporting Information, together with cone voltages and collision energies (collision gas argon, 10-3 mbar). The generalized instrumental parameters were as follows: Capillary voltage, 2.5 kV; drying and nebulizer gas flow (N2), 300 and 20 L/h, respectively; desolvation and source temperature, 150 and 120 °C, respectively. All PFAS determinations were made using the internal standard quantification method employing 13C4PFOA as IS. Concentration values were not corrected for recovery difference between analyte and IS (see also next paragraph). Quality Control. The extraction method employed in the present study (with the exception of the concentration step) has previously been validated for biological matrices and showed excellent analyte recoveries ranging between 90 and 110% for PFCAs from C6 to C14 (22). Including extract concentration, we presently determined recoveries between 70 and 90% for C6- to C10-PFCAs and 65-70% for C11-C14 PFCAs. Extraction efficiencies for PFSs, including PFOSA and 6:2 FTS, were determined to be 70-95%. Furthermore, mean method recoveries ((1 standard error) of the mass labeled compounds 18O2-PFOS and 13C4-PFOA were 74 ( 1.3 and 74 ( 1.4% (n ) 30), respectively. Based on the consistency of these results, 13C4-PFOA was chosen as IS for quantification of all target compounds. Method limits of quantification (MLOQs) (Table S2, Supporting Information) for all analytes were determined based on four blank extraction experiments. In a situation of detectable blank contamination (i.e., for perfluorohexanoate (PFHxA) and -heptanoate (PFHpA)), the MLOQs were defined as the quantified average blank signal plus three standard deviations. For all other analytes, MLOQs were based on a signal-to-noise ratio of 10 in blank extraction chromatograms at the time point of elution of the given analyte. A fish tissue sample used in an international interlaboratory comparison (ILC) study in 2005 (23) was analyzed along with the egg samples. The obtained concentrations deviated from the median concentration from the ILC study by 67% for PFOSA (however, median and mean of the ILC differed by more than a factor of 2), 37% for perfluorododecanoate (PFDoA) and less than 22% for all other compounds quantified in the ILC (i.e., PFHxA, PFHpA, PFOA, perfluorononanoate (PFNA), -decanoate (PFDcA), -undecanoate (PFUnA), perfluorobutane sulfonate (PFBS), -hexane sulfonate (PFHxS), and PFOS). Data Analysis. The differences in PFCA patterns in eggs of herring gulls between the sampling sites (Hornøya and Røst) and collection years (1983, 1993, and 2003) were

investigated using principal component (PC) analysis. This was done by extracting PCs from the relative proportions of eight PFCAs (PFOA, PFNA, PFDcA, PFUnA, PFDoA, perfluorotridenanoate (PFTriA), -tetradecanoate (PFTeA), and -pentadecanoate (PFPeA)) detected in 60% or more of the egg samples to the summed PFCA concentrations (Σ8PFCA). For those PFCAs detectable in at least 60% of the samples, the concentrations below the MLOQs were assigned a randomly generated value between zero and the compound-specific MLOQs (Table S2, Supporting Information). PCs with eigenvalues above 1 were considered to account for a significant contribution to the total variance according to the latent root criterion (24). Compounds with correlation coefficients (i.e., factor loadings) greater than (0.65 on any PC were considered significant (24). Factor loading rotation was computed using Varimax to give a clearer graphical separation of the PCs. The differences between sampling sites and collection years in compound concentrations (log-transformed) and proportions were investigated using the analysis of variance (ANOVA), followed by the Fisher post-hoc test. Correlations between two variables were expressed using the Pearson coefficient r. The statistical package utilized was Statistica (StatSoft, Tulsa, OK), and the level of significance was set at 0.05.

Results and Discussion PFAS Concentrations and Patterns. Whole eggs of herring gulls from two colonies in Northern Norway were monitored for four PFSs (PFBS, PFHxS, PFOS, and perfluorodecane sulfonate (PFDcS)), 6:2 FTS, PFOSA as well as ten PFCAs with chain-lengths between six and fifteen carbons (Table S1, Supporting Information). Concentrations of individual PFAS and sums of closely related compounds (i.e., Σ4PFS and Σ10PFCA) determined in eggs, grouped based on colony (Hornøya and Røst) and year (1983, 1993, and 2003), are listed in Table S2 (Supporting Information). Typical chromatograms of a herring gull egg sample (Røst, 2003) are shown in Figure S2 (Supporting Information). PFOS was consistently and by far the most abundant fluorochemical quantified in herring gull eggs from Northern Norway with concentrations up to 52 ng/g ww (Hornøya, 2003). Such large dominance of PFOS was in accordance with other reports of PFAS in seabird eggs from Northern Europe: e.g., common guillemots from the Baltic Sea (9) and glaucous gulls (Larus hyperboreus) from Svalbard in the Norwegian Arctic (6), and in wildlife in general (8). Among the other PFSs analyzed, PFBS was below detection in all egg samples, whereas PFHxS and PFDcS were found at concentrations several orders of magnitude lower than PFOS. When combined, the concentrations of PFHxS and PFDcS made up approximately 2% of Σ4PFS. The highest mean PFOS concentration in herring gull eggs from Røst 2003 (42 ng/g ww; Table S2, Supporting Information) was roughly 3- and 15-fold lower compared to eggs of Svalbard glaucous gulls collected in 2004 (n ) 10; mean: 104 ng/g ww) (6) and eggs of Baltic Sea common guillemots collected in 2003 (n ) 9; mean: 614 ng/g ww) (9), respectively. However, comparisons among seabirds, or any other avian species, in organohalogen exposure and accumulation should always be made with caution due to interspecies differences in feeding ecology. While common guillemots from the Baltic Sea are exclusive pelagic fish feeders, herring gulls and glaucous gulls from Norway and Svalbard, respectively, exhibit a more analogous opportunistic diet composed mainly of fish, but also crustaceans, seabird chicks, and eggs. However, as shown in a study of glaucous gulls from Svalbard, important individual differences in feeding ecology may be found between neighboring nesting colonies (i.e., predominantly fish-feeders versus predators on seabird chicks and eggs) (25), which may, in part, explain current PFOS concentration differences between herring gulls and glaucous gulls.

PFOSA was detected in 77% of the herring gull eggs at concentrations up to 427 pg/g ww (Hornøya, 2003). The limited occurrence of PFOSA in herring gull eggs may reflect the low background levels reported in the Norwegian environment (26). Furthermore, specific toxicokinetic factor such as metabolism (i.e., partial degradation to PFOS) (27, 28) may have played a role in the retention, mobilization, and maternal transfer of PFOSA in herring gulls. By analogy, the occurrence of PFOSA could not be confirmed in Svalbard glaucous gull eggs (6), although in this survey the instrumental limit of detection (1.92 ng/g ww) was notably higher compared to that of the present study (Table S2, Supporting Information). The 6:2 FTS, a possible degradation product of fluorotelomer-based aqueous fire-fighting foam agents, was below the established MLOQ in virtually all egg samples. The general profile of PFCAs in herring gull eggs was characterized by high proportions of odd and long carbonchain length compounds, in which the PFUnA (C11; highest mean 4.2 ng/g ww, Hornøya 2003) and PFTriA (C13; highest mean 2.8 ng/g ww, Røst 1993) were the most dominant analytes (e.g., Røst egg samples: Figure S3, Supporting Information). This PFCA pattern has been reported in tissues and blood of mammalian wildlife and other avian species (8), as well as in eggs of Svalbard glaucous gulls (6). However, the origin of this pattern remains to be confirmed as almost exclusively PFOA or PFNA were produced industrially (95% of the industry-wide PFCA emissions estimated in 2000) (29). Nonetheless, PFOA and PFNA products, depending upon the synthesis route and raw material, are known to contain more bioaccumulative, longer carbon-chain impurities (PFCAs up to C15 have been identified), which may partly explain their ubiquitous presence in wildlife and human samples (29). Moreover, it has been suggested that the oxidative atmospheric (30, 31) and biological (32, 33) degradation of volatile polyfluorinated precursor compounds (mainly fluorotelomer alcohols) is a potential source of PFCA loadings in animals, including those inhabiting the remote Arctic regions. In fact, the predominant odd carbon-chain PFCA pattern may be the result of degradation of fluorotelomerbased precursors, which exclusively contain even carbonchain homologues. The C6- and C7-chain compounds PFHxA and PFHpA, respectively, were not detected in any of the herring gull eggs. Worthwhile to note are the substantially higher MLOQs for PFHxA and PFHpA relative to the longer carbon-chain length PFCAs (Table S2, Supporting Information), which were a result of blank contamination for these compounds. Concentrations of Σ10PFCA in herring gull eggs co-varied positively with those of Σ4PFS (r2 ) 0.81; p < 0.0001), which may be the result of similar temporal variation for these two compound classes. However, current Σ10PFCA concentrations were on average 81% (range: 70-90%) lower compared to Σ4PFS. This may be indicative of limited environmental exposure to PFCAs in herring gulls relative to PFSs as a result of low background levels in Norway, and by extension in Scandinavia. In fact, a comprehensive survey of PFHxA, PFHpA, PFOA, and PFNA in water samples of 14 major rivers across the EU countries showed these compounds occurred at the lowest levels in Sweden based on measurement in three rivers (34). Temporal Trends. A 3-point temporal trend was investigated for PFAS concentrations in herring gull eggs collected in 1983, 1993, and 2003. Results for selected PFSs (PFOS and PFDcS) and PFCAs (PFUnA and PFTriA) are shown in Figure 1. In eggs of the two colonies monitored, PFOS concentrations showed a nearly 2-fold significant increase from 1983 to 1993 (p e 0.04). Comparable increases during this decade also were observed for PFDcS (p e 0.01) in both colonies, and for PFHxS in Røst (p ) 0.0001). Due to the limited number of samples collected and time-points investigated in the present VOL. 41, NO. 19, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 1. Temporal changes (1983, 1993, and 2003) of PFOS, PFDcS, PFUnA, and PFTriA concentrations (pg/g ww) in eggs of herring gulls collected from Hornøya and Røst. Concentration means are shown with 95% confidence intervals. study, no compound doubling time could be calculated. Nonetheless, the relatively steep increase of PFOS residues in herring gull eggs from 1983 to 1993 agreed well with other investigations in biota samples archived during an analogous time window (i.e., from the early 1980s to early 1990s) in Northern Europe, Greenland, and the North American Arctic. For instance, Holmstro¨m et al. (9) reported a doubling time of 7-10 years for PFOS in common guillemot eggs from the Baltic Sea, while in liver of ringed seals from Western Greenland (Qeqertarsuaq) (11) and polar bears from the Eastern Canadian Arctic (Baffin Island) (13) doubling times of 10.2 and 9.8 years, respectively, were reported. PFOS levels in present herring gull eggs indicated a leveling off from 1993 to 2003, which also agreed well with observations in liver of Western Greenland ringed seals between 1994 and 2003 (11) and Eastern Canadian Arctic polar bears between 1993 and 2002 (13). Nevertheless, a different trend to PFOS (and PFHxS) was observed for PFDcS concentrations in herring gull egg samples for which an upward slope was observed throughout the entire study period (Figure 1). The reasons for the increase of PFDcS in herring gull eggs from Northern Norway post1993 are as yet unclear. There is, to our knowledge, no other study that has reported the temporal variations of this C10PFS in biota samples, or in the environment. Similar to the presently monitored PFSs, the C8- to C13PFCA concentrations in Hørnøya and Røst eggs showed significant increases between 1983 and 1993 (p e 0.01), with the exception of PFOA in Hørnøya (p ) 0.20), followed either by an increase post-1993 (PFOA, PFNA, PFDcA, and PFUnA), although nonsignificant, or an apparent leveling off (PFDoA and PFTriA). Significant temporal increases were also observed for PFNA, PFDcA, and PFUnA levels in liver of Canadian Arctic ringed seals (12) and polar bears (13) that were analyzed up to 2004 and 2002, respectively. Taken together, these data may reflect the ongoing large volume usage and environmental inputs in Norway and northern regions of North America of PFOA and PFNA mixtures and associated longer carbon-chain impurities, as well as possible 6674

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PFCA precursor compounds such as the fluorotelomer alcohols and olefins. Spatial Trends. Mean concentrations of individual PFAS compounds in herring gull eggs generally were not different between the two colonies when sampling year was included as covariable, with the exception of PFHxS (1993; p ) 0.003), PFOA (1993 and 2003; p < 0.0001) (see also next paragraph) and PFNA (1993; p ) 0.001) that were highest in the southernmost colony, Røst. A general absence of spatial gradient also was reported for six polybrominated diphenyl ether (PBDE) congeners determined in the same herring gull eggs as those analyzed in the present study (20). Interestingly, in the study of Knudsen et al. (20), the standard error of the mean Σ6PBDE concentrations in herring gull eggs represented on average 20% of the mean Σ6PBDE in the two colonies investigated (1983, 1993, and 2003 samples), whereas in the present study this proportion was 14% for Σ4PFS and Σ10PFCA. This may indicate a lower population variance for egg concentrations of PFAS, which are predominantly associated to the protein pool (35), relative to the typically lipophilic substances such as the PBDEs. In line with these findings, a correspondingly lower variability in PFOS concentrations compared to PBDEs was reported for guillemot eggs (9). This may suggest that less variable physiological parameters than the total lipid content govern the retention and maternal transfer of PFAS in bird eggs (e.g., protein type, content, and PFAS affinity). The proportions of eight individual PFCAs (C8 to C15) to Σ8PFCA concentrations were compared between the colonies and sampling years using PC 1 and PC 2 (Figure 2). Eggs from Røst sampled in 1993 and 2003 were characterized by significantly higher proportions (ANOVA; p e 0.0001) of PFOA compared to Hørnøya samples collected during those years, which may point out proximal sources of PFOA in this coastal region of Northern Norway. These findings were supported by a comprehensive survey undertaken in Atlantic cod liver samples collected at various sites along the Norwegian coast in which remarkably high proportions of PFOA were reported

FIGURE 2. Proportions of eight individual PFCAs to the summed PFCA (Σ8PFCA) concentrations extracted using principal component (PC) analysis. The two first PCs, PC 1, and PC 2, are plotted. Mean ((1 standard error) factor scores (lower biplot) are shown for individual sampling colonies and collection years of herring gull eggs from Northern Norway. The percent variability explained by PC 1 and PC 2 is provided. in samples from a nearby location (Svolvær) (26). Alternatively, a higher occurrence of PFOA in Røst eggs (1993 and 2003 samples) relative to those from Hornøya may be the partial result of an enhanced contribution from oceanic transport. In fact, along the west coast of Norway runs the Gulf Stream, which may contribute to substantial southernsourced inputs of PFOA (and PFNA and PFHxS, see, also, the preceding paragraph) in Røst, but to a more limited extent in the region encompassing Hornøya. By comparison with Hornøya and the other sampling years in Røst, Røst eggs collected in 1993 contained generally higher proportions of the C14- and C15-PFCAs (PFTeA and PFPeA). In general, eggs from Hornøya exhibited less of a temporal variation in PFCA compositional profile compared to Røst (see, also, Figure S3, Supporting Information). Worthwhile to note is that in Hornøya eggs (1983, 1993, and 2003 samples) somewhat higher proportions of PFDcA and PFUnA were found. Present results suggest that direct and indirect local- and/ or remote-sourced inputs (atmospheric and waterborne) of PFCAs have changed over the last two decades in those two geographically distinct areas of Northern Norway. This may also suggest that prevailing local conditions (e.g., ambient air temperature and humidity, wind, airborne organic particle size, and content and oceanic currents) at those two sites have had certain impacts on the transport pathways and fate of PFCAs and/or their potential volatile precursor compounds (e.g., fluorotelomer alcohols and olefins). In fact, it has been suggested that several atmospheric (and biological) factors influence the global dissemination, partitioning, sorption and degradation of airborne PFCA precursors (29). Additionally, it can be postulated that in herring gulls, PFCAs have partitioning and uptake/clearance rates that vary as a function of their carbon-chain lengths as, for example, shown in rainbow trout (36), which, in turn, may influence their maternal mobilization and deposition into eggs. Alternatively,

a shift in dietary preferences of adult herring gulls could also explain this temporal variation in PFCA patterns among eggs from Røst and Hornøya. This hypothesis was put forward by the group of Holmstro¨m et al. (9) to explain the possible decrease in PFOS levels in common guillemot eggs after a sharp peak in 1997. Although time-dependent fluctuations in diet composition are as yet not documented in herring gull populations from Northern Norway, retrospective analyses involving ecological tracers, i.e., stable nitrogen isotopes and fatty acids, have demonstrated such changes in herring gull colonies from the North American Great Lakes (37). Toxicological Implications. Recently, acute and chronic dietary exposure studies with PFOS in mallard ducks (Anas platyrhynchos) and northern bobwhite quails (Colinus virginianus) (38, 39) have led to calculation of PFOS toxicity reference values (TRVs) and predicted no effect concentrations (PNECs) based on the characteristics of top avian predators (e.g., birds of prey and certain gull species) (40). Conservative egg yolk-based TRVs and PNECs were determined as 1.7 and 1.0 µg PFOS/mL, respectively. In that same study, the lowest observable adverse effect level (LOAEL) in egg yolk was 62.0 µg PFOS/mL. Hence, the most recent (and highest) mean PFOS concentration in herring gull eggs from Northern Norway was roughly 43, 25, and 1566 times lower than the PFOS TRV, PNEC, and LOAEL values, respectively. From a toxicological standpoint, and assuming the sensitivities to PFOS exposure in mallard ducks and northern bobwhite quails also apply to herring gulls, recent concentrations in eggs suggest that PFOS alone would pose a minimal risk to the developing herring gull embryo. However, PFOS and other accumulated PFAS in herring gulls need to be assessed as part of a broad contaminant cocktail having health risk potential (38-42), including chlorine- and brominebased chemicals (18-20). Moreover, seabird eggs are part of the traditional human diet in Northern Norway, and particular attention should be drawn on the potential shortand long-term health risks for humans associated with their frequent (seasonal) consumption.

Acknowledgments We thank Tycho Anker-Nilssen, Geir Helge Systad, Rob Barrett, and Statskog for their assistance with collection of the eggs, Anuschka Polder for sample processing and preparation, as well as Robert J. Letcher for insightful comments on the manuscript. This study received financial support from the Norwegian Pollution Control Authority and the Ecotoxicology Programme of the Norwegian Polar Institute.

Supporting Information Available Additional information on reference standard compounds, instrumental methods, method limits of quantification, concentrations of individual PFAS determined, sampling sites, typical chromatograms, and composition of individual PFCAs to Σ8PFCA is provided. This material is available free of charge via the Internet at http://pubs.acs.org.

Literature Cited (1) OSPAR Commission. OSPAR Background Document on perfluorooctane Sulfonate (update 2006), publication number: 269/ 2006; Oslo Paris (OSPAR) Commission: London, UK. 2006; http://www.ospar.org/eng/html/welcome.html. (2) UNEP. Draft Risk Profile: Perfluorooctane Sulfonate (PFOS), publication number: UNEP/POPS/POPRC.2/11; United Nations Environment Program (UNEP), Stockholm Convention on Persistent Organic Pollutants, Persistent Organic Pollutants Review Committee, Second meeting, Geneva, Switzerland, 2006; http://www.unon.org/confss/doc/unep/pops/POPRC_02/ POPRC_02.HTM. (3) EU. Directive 2006/122/EC of the European Parliament and of the Council, Strasbourg, France, December 12, 2006; http:// VOL. 41, NO. 19, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Received for review March 23, 2007. Revised manuscript received July 17, 2007. Accepted July 24, 2007. ES070723J

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