Organochlorine Compounds and Their Metabolites in Seven Icelandic

Mar 31, 2010 - Iceland is located in the sub-Arctic part of the North Atlantic, ...... G. W. New organochlorine contaminants and metabolites in plasma...
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Environ. Sci. Technol. 2010, 44, 3252–3259

Organochlorine Compounds and Their Metabolites in Seven Icelandic Seabird Species - a Comparative Study ¨ NN JO ¨ RUNDSDO ´ T T I R , * ,† HRO ¨ FSTRAND,† KARIN LO ¨ RUNDUR SVAVARSSON,‡ JO ANDERS BIGNERT,§ AND ÅKE BERGMAN† Environmental Chemistry Unit, Department of Materials and Environmental Chemistry, Stockholm University, SE-106 91 Stockholm, Sweden, Institute of Biology, University of Iceland, Aragata 9, 101 Reykjavı´k, Iceland, and Department of Contaminant Research, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden

Received September 17, 2009. Revised manuscript received March 14, 2010. Accepted March 19, 2010.

The present study is designed to assess the occurrence of a few organochlorine contaminants and their metabolites in eggs of different marine bird species in Iceland, a country located in the sub-Arctic of the North-Western Atlantic. Previous investigations from e.g. Sweden and The Netherlands have shown some obvious differences in contaminant concentrations, including e.g. hydroxylated polychlorinated biphenyl metabolites (OH-PCBs) in guillemot (Uria aalge) and other bird species. Eggs from seven marine bird species, Arctic tern (Sterna paradisaea), common eider (Somateria mollissima), guillemot, fulmar (Fulmarus glacialis), great black-backed gull (Larus marinus), lesser black-backed gull (Larus fuscus), and great skua (Stercorarius skua), that all breed in Iceland, were collected and analyzed for several persistent organic compounds and their metabolites. The contaminant levels varied between the species investigated. The highest concentrations were found in eggs from the great skua (18 and 23 µg/g l.w. of CB-153 and 4,4′DDE, respectively). The concentration difference was generally 2 orders of magnitude higher in great skua for all organochlorine compounds analyzed with the exception of HCB. HCB did not vary as much between the seven species (ranging from 34 to 710 ng/g l.w). OH-PCB and MeSO2-PCB metabolites congener concentrations and patterns showed differences in metabolic capacity between bird species. Guillemot and great skua seem to distinguish themselves most from other species i.e. with the absence of 4-OH-CB187 and low relative levels of 4-OH-CB146 in guillemot and the low abundance of OH-PCBs in great skua.

Introduction Polychlorinated biphenyls (PCBs) and 1,1,1-trichloro-2,2bis(4-chlorophenyl)ethane (4,4′-DDT) are widespread in the * Corresponding author phone: +354 422 5112; fax: +354 422 5001; e-mail: [email protected]. Current address: Matı´s, Icelandic Food and Biotech R&D, Vı´nlandsleid 12, 113 Reykjavı´k, Iceland. † Stockholm University. ‡ University of Iceland. § Swedish Museum of Natural History. 3252

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environment and have been extensively assessed in the Northern hemisphere for almost half a century, in air, sediment, and biota. Particularly extensive studies have been pursued in the Baltic Sea and the Great Lakes, monitoring guillemot (Uria aalge) (1-5) and herring gull (Larus argentatus), respectively (6-9). The spatial distribution of PCB and 1,1-dichloro-2,2-bis(4-chlorophenyl)ethane (4,4′-DDE) may be exemplified with significantly elevated levels in guillemot eggs from the Baltic Sea and an order of magnitude lower concentration in eggs from the North-Atlantic (10). Monitoring data in seabirds from Norway and the Faroe Islands are more sporadic (11-14). Levels of organochlorine compounds (OCs), such as PCBs, 4,4′-DDE, hexachlorobenzene (HCB), and brominated flame retardants, have been reported in fulmar (Fulmarus glacialis) from the Faroe Islands (12), glaucous gulls (Larus hyperboreus) (14), lesser blackbacked gull (15) little auk (Alle alle), Bru ¨ nnich’s guillemot (Uria lomvia), black guillemot, and black-legged kittiwake (Rissa tridactyla) from Norway (11). These data indicate lower levels of OCs in the bird species from the North-West Atlantic than in the Baltic Sea. Iceland is located in the sub-Arctic part of the North Atlantic, midways between Norway and Greenland. Few studies assessing chemical pollutants have hitherto been performed in Iceland and its marine environment (i.e. refs 16-18). These studies, investigating e.g. ptarmigan (Lagopus mutus), black guillemot (Cepphus grille), and Atlantic salmon (Salmo salar), report concentrations ranging from 2 to 900 ng/g lipid weight (l.w.) for ΣDDTs in breast muscle from different terrestrial and marine birds in Iceland, but levels as high as 65000 ng/g l.w. have been reported in gyrfalcon (Falco rusticolus) (16). The present study is aimed to assess the occurrence and levels of some OCs in Iceland (4,4′-DDE, HCB, hexachlorocyclohexane (HCH), trans-nonachlor, bis(4-chlorophenyl) sulfone (BCPS), and PCBs) in eggs from seabirds with partly different feeding habits. In addition, the study identifies and quantifies hydroxylated and methylsulfonyl-substituted metabolites of 4,4′-DDE and PCBs in order to assess any potential differences in metabolic capabilities between the bird species. All compounds, based on effects in mammals including humans (19, 20), may also be of importance in relation to health effects in the birds. Little is known about PCB and DDE metabolites in birds. Only a few studies have been performed investigating avian metabolism, e.g. the efficiency of the cytochrome P450 superfamily as reviewed by Walker (21). Hydroxylated and methyl sulfone metabolites have rarely been analyzed in birds resulting in a large gap of knowledge (3, 22-25). The few studies published have indicated interspecies differences in metabolism (23, 26), in particular for guillemot compared to other bird species (10). The cytochrome P450 is mainly responsible for the metabolism of xenobiotics like PCBs and 4,4′-DDE (27). The CYP1, CYP2, and/or CYP3 isoforms are mainly responsible for metabolizing environmental pollutants in humans (28). The knowledge on avian forms of cytochrome P450 is not as extensive as for mammals, plants, and insects (21). The avian analogue of CYP 1A1 and 1A2 in mammals are CYP 1A4 and 1A5 (29). This suggests that metabolism of xenobiotics may differ between birds and mammals in many ways, both in capacity and number of metabolites.

Materials and Methods Samples. Eggs from guillemot (Uria aalge) and fulmar (Fulmarus glacialis) were collected from the Vestmannaeyjar Islands, South Iceland. Eggs of Arctic tern (Sterna paradisaea), 10.1021/es902812x

 2010 American Chemical Society

Published on Web 03/31/2010

common eider (Somateria mollissima), great black-backed gull (Larus marinus), and lesser black-backed gull (Larus fuscus) were collected near Sandgerdi, South-West of Iceland, and great skua (Stercorarius skua) eggs were collected from the sands near Kvı´sker, South-East Iceland (locations shown in Figure S1 in the Supporting Information). All eggs were collected in the years 2002-2004. The sampling locations were different for the bird species; however, all sampling sites are remote, and therefore site related effect is limited. Difference in long-range transport deposition between the sampling sites is believed to be nonsignificant. No ethical permits are required for egg collection from these species in Iceland. The samples were prepared at the Swedish Museum of Natural History, where the content of the eggs was removed through a drilled hole in the shell. The egg content was thereafter homogenized and stored at -80 °C until taken out for analysis. The bird eggs collected were all from marine species, with some differences in feeding habits, i.e. trophic level. Eiders are a coastal species, staying close to the shore over the winters (30). They feed on benthic species like molluscs and crustaceans (31, 32) and lay about 4-6 eggs (33). Arctic tern is a migrating species, traveling long distances between the hemispheres (30). Iceland is probably the largest breeding site of Arctic tern in the world, with the number of breeding pairs estimated between 250,000 and 500,000 (30). It feeds mostly on sandeel but also on saithe (Pollachius virens) or small crustaceans and even on three-spined stickleback (Gasterosteus aculeatus) and insects (30). The Arctic tern lays 1-3 eggs (34). Guillemots are residential and pelagic birds. The Icelandic guillemots do not leave the ocean around Iceland (30) even though some longer migrations may occur. The guillemot has a varying diet, feeding on e.g. crustaceans, molluscs, sandeel (Ammodytes ssp.), capelin (Mallotus villosus), and herring (Clupea harengus) depending on food availability (35-37). They lay one egg, but a lost egg is commonly replaced within 15 days (38). Fulmars are pelagic but migrate over large areas, i.e. between Northern Canada and Norway (30). They often follow fishing boats and feed on offal (39, 40) but also on Norway pout (Trisopterus esmarkii), clupeids (40), and sandeel (36). They lay one egg (30). Great black-backed gull is a partial pelagic and residential species, but young immature birds tend to migrate to the U.K. over the winter (30). Great black-backed gull has opportunistic feeding habits, feeding on dumpsites, offal from fishing boats, carcasses, and fish. Great black-backed gull is even known to prey on other birds (30, 41), but its reproductive success seems to depend on fish such as herring and capelin (42-45). They usually lay 2-3 eggs (46). Lesser blackbacked gull is migratory, often with wintering areas in equatorial Africa (47, 48). It is a generalist and opportunistic feeder, following fishing boats for offal (49), feeding also on fish and crabs (50). They commonly lay 2-3 eggs (50, 51). Great skua is migratory and migrates long distances to Northwest Africa and South America during winter (30). It is a top predator that depends highly on fish, like sandeel, and fish offal (52, 53). They also attack other birds to steal their food and predate on other bird species (30, 54). They normally lay two eggs (55). Generally, the birds feeding habits change between seasons and depending if they have chicks or not (40, 56). In addition, the diet changes according to food availability, and there is even a difference between chick and adult diet (57). Further, the time spent by migratory birds on Iceland and in the surrounding waters differs between species. Chemicals. All chemicals used in the present study are listed together with source information in the Supporting Information (SI). PCB congeners are numbered according to Ballschmiter et al. (1993) (58), and the abbreviations of OH-

PCBs and MeSO2-PCBs are abbreviated according to Letcher et al. (2000) (59). Instruments. Analysis and quantification of the analytes were performed by gas chromatography (GC) (Varian Star 3400, Palo Alto, California, U.S.A.) equipped with an electron capture detector (ECD) with a split/splitless injector operated in splitless mode. The GC equipment, analytical columns, and temperature program are presented in the SI. Extraction and Clean up Method. The extraction method used is described in detail by Jensen et al. (2003) (60), but due to the small sample amount the solvent volumes were scaled down to 1/10 of the volume presented in the original article. The extractions were performed in test tubes according to Jo¨rundsdo´ttir et al. (2009), where the method is validated for eggs (10). A description of the extraction and clean up method is given in the SI. Quality Control. Blank solvent samples were extracted and analyzed simultaneously with the samples to determine any external contamination. A homogenate sample was used as a reference material and analyzed repeatedly and simultaneously with the samples to determine the quality of the extraction, clean up, and analysis. Volumetric standard was added just prior to GC-analysis to calculate the recovery of the surrogate standards. Limit of quantification (LOQ) of the GC-ECD method for each species was based on the lowest concentration quantified with a signal-to-noise ratio (S/N) of five. LOQs for each compound are indicated as footnotes in the Tables 1, 2, and 3. In cases where samples were below LOQ, the concentration was set to half of the LOQ value for mean and other statistical calculations. All analytes were below LOQ in the blank solvent samples, indicating no external contaminations of the analytes. The reference samples analyzed simultaneously gave results within 10% margin of error for all analytes. The recoveries with (S.D.) were 97% (6.5%) for CB-200, 60% (11%) for the aryl methyl sulfone surrogate standard (MSF-SS), and 92% (11%) for 4-OH-CB193. Statistics. Geometric means were used rather than arithmetic because the concentration showed a right skewed distribution. The normal distribution of the data set was investigated using Kolmogorov-Smirnov. For the PCBs and pesticides, the Kruskal-Wallis test was performed to investigate if the difference in concentration between species is statistically significant (p < 0.05). Principal Component Analysis (PCA) was applied to study differences in congener patterns for the MeSO2-PCB metabolites among the bird species studied to give a better illustrative view of the difference between the bird species. No statistics were calculated for the OH-PCB metabolites due to the large number of nondetects.

Results Geometric mean concentrations of six PCB congeners HCB, β-HCH, 4,4′-DDE, and trans-nonachlor, expressed on a lipid weight basis, are presented in Table 1. Table S2 shows the results of Kruskal-Wallis comparison of the PCB and pesticide concentration in the bird eggs. No significant difference was found in the concentration of eider and Arctic tern eggs as well as there was no significant difference between Arctic tern eggs and guillemot eggs. The concentration of most compounds is significantly higher in eggs of the great skua compared to the other bird species. The largest difference in mean concentration was in the CB-180 concentration between great skua and eider, the difference being 3 orders of magnitude (Table 1). HCB and β-HCH were the only analytes with a more modest variation between the species, but still highest in the great skua, 710 and 76 ng/g l.w., respectively. Fulmar, great black-backed gull, and lesser black-backed gull were all three intermediate in their VOL. 44, NO. 9, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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TABLE 1. Geometric Mean Concentration with Range (ng/g l.w.) of OCs in Different Bird Species from Icelandf

N sampling year migrating/residential CB-101a CB-138 CB-153 CB-180 CB-183b CB-187 ΣPCBc HCB β-HCHd 4,4′-DDE trans-nonachlore

eider

Arctic tern

guillemot

fulmar

10 2003 residential 9.9 (2) (n.d. - 22) 130 (71 - 400) 150 (91 - 450) 35 (17 - 130) 8.9 (8) (n.d. - 40) 32 (18 - 83) 560 34 (24 - 59) 4.2 (2.0 - 6.2) 170 (130 - 260) 22 (9.2 - 49)

6 2003 migrating 19 (10 - 68) 130 (90 - 180) 160 (110 - 200) 54 (41 - 75) 13 (8.5 - 16) 29 (20 - 41) 560 57 (48 - 90) 6.4 (6.1 - 9.9) 280 (270 - 500) 8.1 (1) (n.d. - 13)

10 2002 residential 25 (15 - 99) 360 (250 - 254) 370 (180 - 750) 110 (69 - 200) 38 (24 - 54) 210 (130 - 300) 1800 310 (250 - 360) 10 (6) (n.d. - 24) 1800 (1400 - 2200) 7.0 (6) (n.d. - 23)

10 2002 residential 200 (120 - 320) 760 (470 - 1300) 1800 (1100 - 2700) 1000 (580 - 1400) 180 (100 - 270) 38 (21 - 62) 5400 270 (190 - 380) 5.1 (2) (n.d. - 13) 2800 (1800 - 5400) 190 (120 - 340)

great blackbacked gull

lesser blackbacked gull

great skua

9 2003 residential 270 (8) (n.d. - 590) 1600 (410 - 2800) 1900 (420 - 3400) 710 (160 - 1400) 180 (36 - 370) 370 (98 - 690) 7100 330 (130 - 600) n.d.

8 2003 migrating 75 (7) (n.d. - 140) 1200 (640 - 2300) 1600 (770 - 3000) 900 (320 - 1600) 220 (92 - 350) 430 (200 - 860) 6000 200 (130 - 450) 12 (4.3 - 69) 2100 (940 - 5800) 230 (160 - 420)

10 2004 migrating 1300 (730 - 2500) 9200 (3700 - 32000) 18 000 (6300 - 87 000) 14 000 (5200 - 60000) 2200 (840 - 8100) 2800 (1500 - 13000) 62 000 710 (280 - 1800) 76 (3) (n.d. - 2800) 23 000 (8400 - 100 000) 1700 (830 - 3200)

3300 (840 - 6000) 230 (94 - 780)

a LOQ: 17 ng/g l.w. (eider), 150 ng/g l.w. (great black-backed gull), 66 ng/g l.w. (lesser black-backed gull). b LOQ: 4.3 ng/g l.w. (eider). c ΣPCB: sum of CB-101, CB-105, CB-118, CB-128, CB-138, CB-146, CB-153, CB-156, CB-170, CB-180, CB-183, and CB-187. d LOQ: 8.1 ng/g l.w. (fulmar), 80 ng/g l.w. (great skua). e LOQ: 12 ng/g l.w. (Arctic tern), 7.0 ng/g l.w. (guillemot). f The number in parentheses following the mean (when applied) is number of samples above limit of quantification (LOQ). N is the number of samples from each species.

TABLE 2. Geometric Mean Concentrations with Range (ng/g l.w.) of OH-PCBs in Different Bird Species from Icelandg eider

Arctic tern

a

n.d.

n.d.

b

4-OH-CB146

n.d.

n.d.

3′-OH-CB138c

n.d.

n.d.

3-OH-CB180

n.d.

n.d.

3′-OH-CB187d

n.d.

n.d.

0.50 (0.18 - 1.4) 0.50 0.89 • 10-3

0.38 (5) (n.d. - 0.87) 0.35 0.63 • 10-3

3-OH-CB153

e

4-OH-CB187

ΣOH-PCBf ΣOH-PCB/ΣPCB

great blackbacked gull

lesser blackbacked gull

n.d.

n.d.

n.d.

n.d.

n.d.

n.d.

0.23 (4) (n.d. - 0.93) 1.1 (9) (n.d. - 0.93) n.d.

n.d.

n.d.

n.d.

n.d.

n.d.

n.d.

13 (6.6 - 18) 17 3.1 • 10-3

1.5 (0.36 - 3.7) 1.5 0.21 • 10-3

0.32 (2) (n.d. - 0.71) 0.96 (5) (n.d. - 1.8) 1.3 0.22 • 10-3

guillemot

fulmar

8.3 (4.6 - 16) 0.27 (2) (n.d. - 0.75) 2.1 (1.0 - 4.8) 1.2 (0.69 - 2.1) n.d.

0.63 (0.36 - 1.3) 3.3 (1.6 - 5.6) 0.24 (3) (n.d. - 0.83) n.d.

n.d. 11 6.1 • 10-3

great skua

2.7 (0.98 - 15) 4.0 0.065 • 10-3

a LOQ: 0.26 ng/g l.w. (great skua). b LOQ: 0.43 ng/g l.w. (guillemot), 0.33 ng/g l.w. (great skua). c LOQ: 0.34 ng/g l.w. (fulmar). d LOQ: 1.1 ng/g l.w. (lesser black-backed gull). e LOQ: 0.18 ng/g l.w. (Arctic tern), 0.52 ng/g l.w. (lesser black-backed gull). f ΣOH-PCB: sum of 3-OH-CB153, 4-OH-CB146, 3′-OH-CB138, 3-OH-CB180, 3′-OH-CB187, and 4-OH-CB187. g The number in parentheses following the mean (when applied) is number of samples above limit of quantification (LOQ). N is the number of samples from each species.

concentrations of the analytes with far lower levels than the great skua but also higher than in guillemot, Arctic tern, and eider (Table 1). Concentrations of six OH-PCB metabolites are presented in Table 2; concentrations of eight MeSO2-PCB metabolites and of 3-MeSO2-DDE are presented in Table 3. For OH-PCBs, 4-OH-CB187 is either the only congener detected or the congener present in the highest concentration in eggs of all bird species analyzed, except for guillemot. If other OHPCBs are present, 4-OH-CB187 is followed by either 4-OHCB146 or 3′-OH-CB187. In guillemot eggs, however, 3-OHCB153 is the dominating OH-PCB. 3254

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The congener pattern of MeSO2-PCBs (Figures 1 and 2) also differs between bird species. However, there is not as large a difference in MeSO2-PCB and 3-MeSO2-DDE concentration between the bird species compared to the PCB concentration (Tables 1 and 3). While there is a difference of more than 2 orders of magnitude of 4,4′-DDE in the bird eggs there is only 1 order of magnitude difference in the mean levels of 3-MeSO2-DDE. The lowest concentration of 3-MeSO2-DDE is found in guillemot, fulmar, and eider eggs and the highest concentration in great skua eggs. Still, the great skua is significantly separated from the other species, except for fulmar (Table 3). Although similarities between

TABLE 3. Geometric Mean Concentrations of Methyl Sulfonyl Metabolites of PCB and 4,4′-DDE with Range (ng/g l.w.) in Different Bird Species from Icelandk

a

5-MeSO2-CB64

3′-MeSO2-CB101b 4′-MeSO2-CB101c 4-MeSO2-CB110d 3′-MeSO2-CB141e 4′-MeSO2-CB141f 5-MeSO2-CB149g 4-MeSO2-CB149h sum of MeSO2-PCBI ΣMeSO2-PCB/ΣPCB 3-MeSO2-DDEj

eider

Arctic tern

0.44 (4) (n.d. - 2.6) 0.94 (0.13 - 2.3) 0.33 (2) (n.d. - 1.1) n.d.

1.2 (5) (n.d. - 2.1) 0.95 (3) (n.d. - 1.7) 0.60 (2) (n.d. - 1.3) n.d.

0.79 (4) (n.d. - 6.1) n.d.

1.2 (5) (n.d. - 2.8) n.d.

0.65 (8) (n.d. - 2.2) n.d.

1.3 (0.93 - 1.8) n.d.

3.2 5.7 • 10-3 1.7 (8) (n.d. - 22)

5.3 9.4 • 10-3 2.8 (0.61 - 14)

guillemot

fulmar

n.d. 0.20 (2) (n.d. - 0.44) 0.49 (0.20 - 0.74) 0.28 (5) (n.d. - 0.90) 0.23 (9) (n.d. - 0.36) 0.49 (0.28 - 0.64) 0.28 (8) (n.d. - 0.74) 1.5 (0.93 - 2.6) 3.5 1.9 • 10-3 1.5 (1.0 - 2.0)

3.4 (9) (n.d. - 11) 3.6 (1.7 - 7.5) 1.6 (0.77 - 3) 0.87 (4) (n.d. - 1.3) 0.95 (7) (n.d. - 3.0) 0.39 (4) (n.d. - 1.5) 2.9 (1.4 - 7.3) 0.75 (7) (n.d. - 2.0) 14 2.6 • 10-3 1.6 (0.76 - 5.8)

great blackbacked gull n.d. 2.7 (1.1 - 22) 1.7 (8) (n.d. - 19) 0.82 (8) (n.d. - 8.0) 0.76 (3) (n.d. - 4.4) 0.60 (3) (n.d. - 1.9) 0.76 (7) (n.d. - 1.4) n.d. 7.3 1.0 • 10-3 3.4 (1.8 - 14)

lesser blackbacked gull 0.96 (5) (n.d. - 2.3) 3.2 (1.7 - 5.1) 1.2 (7) (n.d. - 3.2) 1.0 (6) (n.d. - 2.1) 0.88 (5) (n.d. - 2.7) n.d. 2.6 (1.3 - 4.3) 1.2 (4) (n.d. - 5.2) 11 1.8 • 10-3 3.7 (1.4 - 9.5)

great skua 1.5 (5) (n.d. - 4.2) 13 (3.4 - 100) 9.3 (3.8 - 54) 0.81 (6) (n.d. - 1.8) 4.7 (1.5 - 27) 2.3 (1.2 - 8.3) 4.2 (2.0 - 13) 5.1 (3.4 - 13) 41 0.66 • 10-3 11 (6.0 - 28)

a LOQ: 0.43 ng/g l.w. (eider), 0.84 ng/g l.w. (Arctic tern), 1.5 ng/g l.w. (fulmar), 0.85 ng/g l.w. (lesser black-backed gull), 1.2 ng/g l.w. (great skua). b LOQ: 1.2 ng/g l.w. (Arctic tern), 0.33 ng/g l.w. (guillemot). c LOQ: 0.51 ng/g l.w. (eider), 0.88 ng/g l.w. (Arctic tern), 0.70 ng/g l.w. (great black-backed gull), 0.53 ng/g l.w. (lesser black-backed gull). d LOQ: 0.25 ng/g l.w. (guillemot), 2.5 ng/g l.w. (fulmar), 0.34 ng/g l.w. (great black-backed gull), 0.85 ng/g l.w. (lesser black-backed gull), 0.69 ng/g l.w. (great skua). e LOQ: 0.61 ng/g l.w. (eider), 0.78 ng/g l.w. (artic tern), 0.28 ng/g l.w. (guillemot), 0.57 ng/g l.w. (fulmar), 0.97 ng/g l.w. (great black-backed gull), 0.75 ng/g l.w. (lesser black-backed gull). f LOQ: 0.44 ng/g l.w. (fulmar), 0.81 ng/g l.w. (great black-backed gull). g LOQ: 0.20 ng/g l.w. 0.38 ng/g l.w. (eider), (guillemot), 0.55 ng/g l.w. (great black-backed gull). h LOQ: 0.57 ng/g l.w. (fulmar), 0.88 ng/g l.w. (lesser black-backed gull). I ΣMeSO2-PCB: sum of 5-MeSO2-CB64, 3′-MeSO2-CB101, 4′-MeSO2-CB101, 4-MeSO2-CB110, 3′-MeSO2-CB141, 4′-MeSO2-CB141, 5-MeSO2-CB149, 4-MeSO2-CB149. j LOQ: 0.24 ng/g l.w. (eider). k The number in parentheses following the mean (when applied) is number of samples above limit of quantification (LOQ). N is the number of samples from each species.

FIGURE 1. Concentration of each MeSO2-PCB metabolite shown as a percentage of the sum of all MeSO2-PCB metabolites presented in Table 3. the species can be seen for the 3-MeSO2-DDE, the combined MeSO2-congener pattern separates most species almost completely (Figure 2). Further, the great skua eggs contain the highest PCB concentrations and the largest number of metabolites detected, with almost all congeners above LOQ in most samples. Concentrations of BCPS were very low in all samples, close to limit of detection (3 ng/g l.w.), and therefore not reported.

Discussion PCBs, HCB, β-HCH, and 4,4′-DDE. When comparing two pairs of birds, eider/Arctic tern, guillemot/fulmar, and great black-backed gull/lesser black-backed gull, respectively, no significant differences in OC levels are observed. An exception is the trans-nonachlor concentration in the guillemot and fulmar eggs as well as the β-HCH concentration in great blackbacked gull and lesser black-backed gull eggs. This result is VOL. 44, NO. 9, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 2. Principal component analysis (PCA) of MeSO2-PCB metabolites in different bird species, except for guillemot eggs. Two fulmar egg samples were excluded as outliers. The first PC explains 49% and the second explains 16% of the total variation. The centroids of the various species are indicated by larger circles and are surrounded by Hotelling’s 95 confidence ellipses. GBBG is great black-backed gull, LBBG is lesser black-backed gull, A.tern is Arctic tern, and G.skua is great skua. in accordance with their expected similar trophic level, pair wise. Still some minor differences in OC concentrations are observable between the species (Table 1), likely induced by different feeding habits. For example sandeel that feeds on copepods is a large part of the Arctic tern’s diet, where the eider feeds directly on benthic species. This probably places the tern on a slightly higher trophic level compared to the eider. Further, the feeding pattern differs between the lesser black-backed gull, feeding on fish and marine invertebrates, and the great black-backed gull which is a carnivore with habits of inland feeding (61). No obvious influence is observed that may be related to the migration patterns of the species. However, some refined further research, applying stable isotope measurements (62), confirming the trophic level of the birds may show hitherto hidden influences of migration on bioaccumulation. The sum of the mean levels of the 12 major PCB congeners is higher than 60 µg/g l.w., and the concentration of 4,4′DDE is 23 µg/g l.w. in the great skua. The concentrations of these two POPs, both banned decades ago, are surprisingly high. The concentrations are approximately 1-2 orders of magnitude higher in the great skua than in the other bird species in the present study. Similarly high concentrations have been reported in previous studies of Icelandic gyrfalcon (Falco rusticolus) for which breast muscle were analyzed. Concentrations of 53 µg/g l.w of HCB, 147 µg/g l.w. of sum of 21 PCB congeners, and 64 µg/g l.w. of sum of four DDT congeners have been reported (16). No data exist for eggs from the gyrfalcon, making a comparison less exact. Nonetheless, the concentrations in these two top predators are indeed very high for a remote hatching location like Iceland. The high PCB concentration in the great skua indicates that it may be wise to look into the health status of the great skua and their reproductive capacity, since PCBs have been shown to affect the reproductive capability of other marine birds (63). Further, Verreault and co-workers report a relationship between reduction of basal metabolic rate (BMR) and high concentrations of organochlorines like PCBs and DDE in glaucous gull (14). OH-PCB Metabolites. Previous studies on OH-PCBs in birds, i.e. levels in plasma from two species of albatrosses 3256

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(24), fulmar eggs (22), and blood of white tailed sea eagle (25), all report that 4-OH-CB187 is the major OH-PCB metabolite, followed by 4-OH-CB146 and then, 3-OH-CB153. Jaspers et al. (2008) also report 4-OH-CB187 and 4-OH-CB146 as the predominant OH-PCB congeners in livers of different predatory birds from Belgium (23). However, 3′-OH-CB138 was measured in higher concentrations than 4-OH-CB146 in a species of owls, while 3-OH-CB153 did not contribute significantly to the total OH-PCB concentration in the Belgium species investigated (23). In the present study, the fulmar and the great skua eggs follow the pattern of having the 4-OH-CB187 and 4-OH-CB146 as the dominating OHPCB metabolites. The only OH-PCB congener detected in the eider, Arctic tern, and great black-backed gull is 4-OH-CB187. For lesser black-backed gull, the only congener apart from 4-OH-CB187 that is quantified is 3′-OH-CB187. Comparing fulmar and guillemot, the concentration of 4-OH-CB187 is 13 ng/g l.w. in fulmar eggs but is not detected in guillemot eggs. The concentration of CB-187 is 38 ng/g in fulmar eggs compared to 210 ng/g l.w. in guillemot eggs. The lack of 4-OH-CB187 in the guillemot eggs implies that guillemots are unable to metabolize the parent compound CB-187 to 4-OH-CB187. This is supported with a relatively high concentration of CB187 in the guillemot eggs (Table 1). As reported elsewhere (10), the OH-PCB congener pattern in the guillemot differs from the other species, with the highest abundance of 3-OHCB153, followed by 3′-OH-CB138 and 3-OH-CB180. The OHPCB congener pattern found in the great skua eggs are similar to what is found in the fulmar eggs indicating similarities in active metabolic pathways in these two species. However, the metabolic capacity seems to be far less pronounced in the great skua as visualized by the OH-PCB metabolite concentrations in eggs from the two species (Table 2). On the other hand the great skua has an order of magnitude higher PCB concentration compared to the fulmar (Table 1). The OH-PCB concentrations in this top predator indicate that OH-PCBs are not formed to the same degree in great skua compared to fulmar. Two alternative explanations are either that the OH-PCBs commonly retained in blood are

not retained in the great skua or the transfer of OH-PCBs to the egg is different between the two species. Further investigation on the cytochrome P450 enzyme system in avian species is of interest to improve the understanding of differences in metabolism in birds as implied in the present study. The OH-PCB congener pattern and concentrations found in fulmar eggs in the present study are comparable to what has been reported earlier from fulmar eggs from the Faroe Islands (22). Verreault and co-workers (2007) present the sum concentration of 10 different OHPCB and diOH-PCBs in plasma of glaucous gull from the Norwegian Arctic. The reported concentrations of ΣOH-PCB were 1400 ng/g l.w. and 780 ng/g l.w. in male and female glaucous gull, respectively, while the PCB concentration was similar in males and females (73000 ng/g l.w.) (14). Still, it is difficult to compare data on OCs in glaucous gull plasma with the results from the present study, since the mechanism behind transport of xenobiotics between the mother bird and the egg is unknown. In the present study, the ΣOHPCB/ΣPCB ratio in the bird eggs is 2 orders of magnitude lower compared to what is presented by Klasson-Wehler et al. (1998) in plasma of two species of albatrosses. This indicates that the transfer of phenolic compounds to the egg is rather limited (24). Verreault et al. (2005) also report concentrations of OH-PCBs in eggs and plasma of glaucous gull from the Norwegian Arctic, only detecting 3′-OH-CB138 in sufficiently high concentration in the eggs (0.21 ng/g l.w.) (64). This study is comparable to what is found in the fulmar eggs in the present study, further supporting an interspecies difference between birds. More research on the transfer of contaminants and their metabolites between blood and eggs is to be prioritized. MeSO2-PCB and MeSO2-DDE Metabolites. As for OHPCB metabolites, the dominating MeSO2-PCB congener differs depending on the bird species. There is a greater difference between species in the MeSO2-PCB congener pattern compared to the OH-PCBs. In Figure 1, the concentration of each MeSO2-PCB metabolite is calculated as a percentage of the sum of the eight MeSO2-PCB metabolites presented in Table 3. Guillemot differ the most from the other species with MeSO2-CB149 as the dominant metabolite. For the eider, fulmar, gulls, and great skua, 3′-MeSO2-CB101 is the metabolite present in the highest concentration. For Arctic tern, 4-MeSO2-CB110 is the metabolite in the highest concentration but in very similar concentrations as 3′-MeSO2CB101. The difference between the seven species of the individual MeSO2-PCB congeners (Table 3) are sometimes far lower than what is found for the PCBs (Table 1). In fact, 5-MeSO2-CB64 has a somewhat higher mean level in fulmar than in great skua. The 10-fold difference in ΣMeSO2-PCB/ ΣPCB ratio between the Arctic tern, eider, and the great skua (Table 3) indicates a more efficient metabolism of PCBs to PCB methyl sulfones in eider and Arctic tern than in the great skua. As mentioned above, high levels of OCs have been correlated with a reduced metabolic rate (14). Thus, the great skua with the lowest ΣOH-PCB/ΣPCB and ΣMeSO2PCB/ΣPCB may show such effects. The difference in metabolic capacity is further investigated with a PCA plot (Figure 2). The PCA plot depicts the main MeSO2-PCB metabolites in the different bird eggs (Figure 2). Guillemot egg samples are significantly separated from the other species. The fulmar egg samples do not form a distinctive cluster where great skua egg samples fall within the fulmar egg distribution. The great skua eggs are on the other hand completely separated from the other five species. Great black-backed gull egg samples are also well separated where the lesser black-backed gull egg samples are close to the eider and Arctic tern egg samples. No difference can be found between Arctic tern and eider.

When the ratio (ΣPCB-metabolites)/(ΣPCBs) is calculated, the order of the birds species differ depending if the sum of metabolites is sum of OH-PCBs or sum of MeSO2-PCBs. For OH-PCBs, the guillemot has the highest ratio of sum metabolites compared to sum parent compounds, followed by fulmar. For MeSO2-PCBs, the Arctic tern has the highest ratio, followed by eider. This indicates an interspecies difference in metabolic capacity and/or different excretion capacity of the metabolites between the bird species. The formation of PCB- and DDE-methyl sulfones strongly depends on the intestinal microflora and its ability to catalyze the bond scission between carbon and sulfur in cystein congugates of xenobiotics (65, 66). Assuming birds form the aryl methyl sulfone metabolites in a similar way, differences in the intestinal microorganism content in different bird species will influence sulfone metabolite formation. Nevertheless, the present study clearly shows the formation of DDE and PCB methyl sulfone metabolites in the birds as well as the transfer of these metabolites to the bird eggs. It is notable that the MeSO2-PCB concentrations are similar to the OH-PCB levels in the egg. The ovogenesis largely involves the transfer of lipoproteins from maternal tissues to eggs (67), indicating that lipophilic compounds are more efficiently transported to the egg compared to more hydrophilic compounds as the OH-PCBs. This is supporting a more efficient transfer of the neutral lipophilic sulfones to the egg than transfer of the weak acids, the OH-PCBs. The metabolites found in birds in higher trophic levels, like the gulls and the great skua, are a result of both exposure to metabolites through their food and via their own metabolism. Bird species like guillemot, eider, and Arctic tern are probably not exposed to metabolites through their food, since fish, crustaceans, and molluscs only to a minor extent may be able to form such metabolites (68, 69). Thus, the metabolites in these birds originate most likely from the bird itself. Due to the mechanism of PCB methyl sulfone formation, with an epoxide in an unsubstituted meta-/para-position of a PCB congener and with chlorine substituent on both sides of the epoxide, it is a transformation of the most readily metabolized PCB congeners present in PCB mixtures. Accordingly, it is not always even possible to quantify the precursors of the PCB methyl sulfone metabolites. The concentrations of the PCBs and pesticides likely reflect the trophic levels of the seven species. Based on the parent compounds and MeSO2-PCBs, respectively, it is obvious that the great skua is at the highest trophic level of these bird species. The two gull species and the fulmar are at an intermediate trophic level according to both the POP concentrations and PCB methyl sulfone levels, while guillemot is lower. The eider and Arctic tern are both at the lowest trophic level if POP levels are considered. The results presented in this study, especially concerning PCB metabolites, strongly indicate that there is an interspecies difference in metabolic pathways and capacity between bird species. Among the bird species studied we like to stress that the great skua may be exposed to OCs at concentrations close to where toxic responses are to be expected.

Acknowledgments The preparation of samples by Mats Hjelmberg and Henrik Dahlgren, Swedish Museum of Natural History, is acknowledged, and we would like to thank Pa´ll Marvin Jo´nsson for the eggs from Vestmannaeyjar, Ha´lfda´n Bjo¨rnsson for providing eggs from Kvı´sker, and Gunnar Tho´r Hallgrı´msson for providing eggs from Sandgerdi. This study was financially supported by The Nordic council of ministers (Sea and air quality group and Environment monitoring and data group) though a grant to the CAPNE project (A comparative assessment of persistent organic pollutants and their meVOL. 44, NO. 9, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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tabolites, with emphasis on nontraditional contaminants, in the West-Nordic and the Baltic Proper environments).

Supporting Information Available Figure S1 and Tables S1 and S2. This material is available free of charge via the Internet at http://pubs.acs.org.

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