Temporal trends of organochlorines and mercury in seabird eggs from the Canadian Arctic, 1975–2003

Environmental Pollution 148 (2007) 599e613 www.elsevier.com/locate/envpol

Temporal trends of organochlorines and mercury in seabird eggs from the Canadian Arctic, 1975e2003 Birgit M. Braune* Environment Canada, National Wildlife Research Centre, Carleton University, Raven Road, Ottawa, Ontario, K1A 0H3 Canada Received 10 July 2006; received in revised form 17 November 2006; accepted 21 November 2006

Most organochlorines declined in eggs of three Canadian Arctic seabird species but concentrations of mercury and some HCHs continue to increase. Abstract Organochlorine pesticides, PCBs, total mercury and selenium were measured in eggs of thick-billed murres, northern fulmars and black-legged kittiwakes collected from Prince Leopold Island in the Canadian High Arctic between 1975 and 2003. The primary organochlorines found were SPCB, p,p0 -DDE, oxychlordane, and hexachlorobenzene (HCB). Most of organochlorines analyzed showed either significant declines or no significant change between 1975 and 2003 in all three species. However, significant increases were observed for SHCH in the kittiwakes and fulmars, and b-HCH in the murres and fulmars. Mercury increased significantly in eggs of murres and fulmars, whereas mercury in the kittiwakes did not change significantly over the study period. Statistical analyses included stable-nitrogen isotope ratios (d15N) to control for any variation in trophic level over time. Although the contaminant concentrations reported in this study are below published threshold values, mercury and b-HCH concentrations continue to increase suggesting that continued monitoring is warranted. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Seabirds; Canadian Arctic; Organochlorines; Mercury; Temporal trend

1. Introduction Biota at northern latitudes are exposed to a variety of chemical residues that are, for the most part, transported there by air and ocean currents (Macdonald et al., 2000). Unlike metals, persistent organic pollutants are generated entirely from anthropogenic sources (AMAP, 2004). Chemical characteristics, such as volatility and water solubility, determine the potential of an organic chemical to become an arctic contaminant (Wania, 2003, 2006). Although mercury (Hg) occurs naturally in the environment, anthropogenic sources, such as fossil fuel combustion, non-ferrous metal production, and waste incineration, have been postulated to contribute more significantly to

* Tel.: þ1 613 998 6694; fax: þ1 613 998 0458. E-mail address: [email protected] 0269-7491/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2006.11.024

the occurrence of Hg in the Arctic than natural emissions (AMAP, 2005). Elemental Hg is highly volatile, and gaseous Hg0 partitions readily into the atmosphere where it can undergo long-range atmospheric transport. Due to a complex set of factors (Macdonald et al., 2005), polar regions have become global sinks for Hg. Persistent organochlorine contaminants and Hg biomagnify up the food chain (Braune et al., 2005) making those species feeding at high trophic positions more vulnerable to contaminant exposure via their diet (Borga˚ et al., 2004; Hop et al., 2002). Seabirds feed at relatively high trophic positions in arctic marine food webs (Hobson et al., 2002; Hop et al., 2002) and, therefore, eggs of seabirds have been used to monitor contamination of the marine environment in the Canadian Arctic since 1975 (Braune et al., 2001). At the time of egg formation, the lipophilic organochlorine compounds are transferred along with fat to the eggs (Mineau et al., 1984) thus reflecting

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B.M. Braune / Environmental Pollution 148 (2007) 599e613

the contaminant burden in the female at the time of laying (Braune and Norstrom, 1989). Both mercury and selenium are also readily transferred to the eggs (Ohlendorf, 2003; Wiener et al., 2003). Contaminant burdens in the egg reflect residues assimilated over a long time period by the female and, particularly in migratory species, may integrate exposure from a number of different locations (Hebert, 1998; Monteiro et al., 1999). Few long-term data sets exist to give a clear picture of how concentrations of contaminants have changed temporally at northern latitudes. This is especially true for High Arctic food webs (Barrett et al., 1996). For example, Bignert et al. (2004) have demonstrated that the majority of time-series data sets for Hg in arctic biota are too short to detect temporal trends with an acceptable statistical power. Nevertheless, the available data sets provide strong evidence that the majority of legacy persistent organic pollutants (e.g. PCBs, DDT) have significantly declined in Canadian Arctic biota over the last several decades whereas contaminants such as the hexachlorocyclohexanes (HCHs) and Hg have either remained relatively constant or increased in a number of arctic species (Braune et al., 2005). Interpretation of contaminant concentrations in biota may be confounded if populations vary their diet over trophic levels through time (e.g. see Hebert et al., 1997, 2000). Determination of trophic level in seabirds is possible through the measurement of naturally occurring stable isotopes of nitrogen (15N/14N) (Hebert et al., 1999b; Hobson and Welch, 1992; Hobson et al., 1994). This is also true of seabird eggs since stable isotope ratios in egg material are expected to reflect the diet of the female prior to or during egg-laying (Hebert et al., 1999b; Hobson, 1995). In this paper, the time-series data previously reported by Braune et al. (2001) for the legacy organochlorines and Hg in Canadian Arctic seabirds is extended, and the contaminant trends examined, taking into consideration data on stable isotopes of nitrogen, as a reflection of possible temporal changes in trophic position, which could affect the concentrations of contaminants found in the eggs. 2. Methods 2.1. Sample collection and storage Eggs of black-legged kittiwakes (Rissa tridactyla), northern fulmars (Fulmarus glacialis) and thick-billed murres (Uria lomvia) were collected by hand from the Prince Leopold Island Migratory Bird Sanctuary (74 020 N, 90 050 W) in Lancaster Sound, Nunavut, Canada (Fig. 1) during 1975, 1976, 1977, 1987, 1988, 1993, 1998 and 2003. Sampling years varied slightly for each species and are indicated in Tables 1e4. Each egg was removed from a different nest to maintain independence among samples. Eggs were kept cool in the field and shipped to the National Wildlife Research Centre (NWRC) for processing and residue analyses. Egg contents were homogenized and stored frozen (40  C) in either acetoneehexane rinsed glass vials for subsequent organochlorine analysis or in acid-rinsed polyethylene vials for metals analysis. This method of storage has been tested for evaporative losses of organochlorine compounds over time (Norstrom and Won, 1985) and, since no significant losses were detected at temperatures up to 28  C, has been recommended for long-term preservation of biological specimens. In a study comparing organochlorine residues in eggs of

Greenland

Prince Leopold Island Ba

ffin

Isla nd

Canada Hudson Bay

Fig. 1. Location of sampling site in the Canadian Arctic.

red-breasted mergansers between 1977e1978 and 1990, Heinz et al. (1994) also found that egg samples had sustained no moisture loss over 12 years of frozen storage and that differences in results between the original analyses and the reanalyses were, with the exception of toxaphene, inconsequential. As well, arctic seabird egg samples (n ¼ 11) collected for this study in 1993 and stored in both glass and polyethylene vials were reanalyzed for total mercury in 1998 and again in 2004. Analysis of variance (ANOVA) indicated that there were no significant effects ( p > 0.05) related to storage container or storage time. Samples collected in 1998 and 2003 were analyzed for organochlorines within 6 months of collection. Likewise, samples collected in 1993, 1998 and 2003 were analyzed for mercury and selenium within 6 months of collection. All other samples were retrieved from the Canadian Wildlife Service (CWS) Specimen Bank at NWRC and analyzed retrospectively during 1998e1999 in order to standardize pooling and analytical protocols which varied over earlier years of sampling.

2.2. Organochlorine analysis Egg homogenates were analyzed as pooled (composite) samples with each pool consisting of three individual egg samples. The number of eggs collected in each year dictated the number of pools analyzed. Sample sizes for each year are given in Tables 1e4. Organochlorine analyses of the pooled samples included determination of chlorobenzenes (SCBz ¼ 1,2,4,5-tetrachlorobenzene, 1,2,3,4-tetrachlorobenzene, pentachlorobenzene and hexachlorobenzene), hexachlorocyclohexanes (SHCH ¼ a-, b- and g-hexachlorocyclohexane), chlordane-related compounds (SCHLOR ¼ oxychlordane, trans-chlordane, cis-chlordane, trans-nonachlor, cis-nonachlor and heptachlor epoxide), DDT and its metabolites (SDDT ¼ p,p0-DDE, p,p0 -DDD and p,p0 -DDT), octachlorostyrene (OCS), mirex (SMirex ¼ photomirex and mirex), dieldrin and PCB congeners (SPCB). SPCB consisted of 68 congeners identified according to IUPAC numbers (Ballschmiter et al., 1992) and included congener numbers 16/32, 17, 18, 20/33, 22, 28, 31, 42, 44, 47/48, 49, 52, 56/60, 64/41, 66, 70/76, 74, 85, 87, 90/101, 92, 95, 97, 99, 105, 110, 118, 128, 130, 137, 138, 141, 146, 149, 151, 153, 156, 157, 158, 170/190, 171, 172, 174, 176, 177, 178, 179, 180, 183, 187, 194, 195, 196/203, 200, 199, 202, 206, 207, and 208. Congeners separated by a slash co-eluted during the chromatography process and are therefore reported together. Analysis of samples for organochlorines was carried out at NWRC by gas chromatography using a mass selective detector (GC/MSD) according to CWS Method No. MET-CHEM-OC-04 (Won et al., 2000). Briefly, samples were ground with anhydrous sodium sulfate, transferred to a chromatographic

B.M. Braune / Environmental Pollution 148 (2007) 599e613

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Table 1 Mean concentrations (mg g1 dry weight  standard error) of total mercury (Hg) and selenium (Se) as well as stable-nitrogen isotope ratios (d15N as &  standard error) in eggs of black-legged kittiwakes, northern fulmars and thick-billed murres collected between 1975 and 2003 from Prince Leopold Island Species

Year

n (no. pools)

d15N

% Moisture

Hg

Se

Black-legged kittiwake

1975 1976 1987 1993 1998 2003 p

12 6 3 15 15 12

(4) (2) (1) (5) (5) (4)

15.0  0.2 14.8 15.5 14.1  0.1 15.0  0.1 16.7  0.2

70.0  1.4 76.3 74.8 77.2  0.2 73.7  2.1 76.4  0.4

0.39  0.03 0.78 0.88 0.62  0.05 0.64  0.07 0.82  0.05 ns

3.44  0.16 3.50 3.65 4.38  0.36 2.43  0.15 3.72  0.04 ns

Northern fulmar

1975 1976 1977 1987 1993 1998 2003 p R2adj

15 12 15 6 15 15 15

(5) (4) (5) (2) (5) (5) (5)

13.4  0.1 13.2  0.2 13.1  0.1 13.3 13.0  0.1 13.5  0.1 13.5  0.1

70.2  1.2 69.4  0.7 69.2  1.2 70.7 72.6  1.5 73.3  0.3 74.1  0.3

0.86  0.07 1.06  0.17 0.74  0.07 1.13 1.19  0.09 1.36  0.14 1.41  0.05 <0.0001 0.50

4.45  0.15 4.17  0.19 4.27  0.18 4.09 4.01  0.26 3.34  0.24 4.49  0.23 ns

Thick-billed murre

1975 1976 1977 1987 1988 1993 1998 2003 p R2adj

9 9 9 9 9 15 15 15

(3) (3) (3) (3) (3) (5) (5) (5)

14.9  0.3 15.7  0.3 14.8  0.1 15.8  0.3 15.5  0.5 14.9  0.2 15.5  0.1 15.5  0.1

66.6  1.6 69.7  0.7 67.4  1.8 72.6  1.1 72.4  1.1 73.2  0.5 72.2  0.3 72.0  0.3

0.60  0.01 0.78  0.06 0.46  0.04 0.98  0.06 0.97  0.03 1.13  0.10 1.19  0.07 1.33  0.13 <0.00001 0.70

2.95  0.21 2.57  0.10 2.52  0.28 2.44  0.15 2.90  0.34 2.57  0.14 2.20  0.20 3.01  0.16 ns

Significant or non-significant (ns, p > 0.05) time trends for Hg and Se concentrations are indicated as determined by multiple linear regression analysis controlling for d15N. The adjusted R2 is given for the whole model using year and d15N as regressors. The number of eggs (n) is given with the number of egg pools shown in brackets. column and eluted with solvent. Extracts were cleaned up and fractionated by column chromatography. All samples were spiked with 13C-labelled internal standards (chlorobenzenes, PCB congeners) prior to extraction. Samples were analyzed using a gas chromatograph (GC) coupled with a mass selective detector (MSD) run in selected ion monitoring (SIM) mode. Typical internal standard recoveries are between 70% and 95% for most PCBs and organochlorines, and over 60% for the highly volatile compounds (i.e. chlorobenzenes). Blanks and CWS in-house reference material (HGQA) (Wakeford and Turle, 1997) were run for quality control. The nominal detection limit was 0.1 ng g1 wet weight. Residues were not corrected for internal standard recoveries. It has been shown that the percent lipid level of the total egg contents decreases during incubation whereas the percent water remains relatively constant (Peakall and Gilman, 1979). Given that the degree of incubation of the sampled eggs is not known and may vary from year to year, and that the precision of lipid measurement in egg reference material (HGQA) by gravimetric methodology has been calculated (as the coefficient of variation) to vary by 7e10% (Wakeford and Turle, 1997), organochlorine residue concentrations are reported on a wet weight basis.

2.3. Metals analysis Samples collected in 1998 or earlier were analyzed for total mercury (Hg) according to CWS Method No. MET-CHEM-AA-03 (Neugebauer et al., 2000) and all samples were analyzed for selenium (Se) according to CWS Method No. MET-CHEM-AA-02 (Neugebauer et al., 2000). Samples were thawed, freeze-dried and digested in mineral acids prior to analysis. Selenium was analyzed in all samples by graphite furnace spectrometry (GFAAS) using a Perkin Elmer 3030b equipped with deuterium background corrector, HGA-300 graphite furnace and AS-40 autosampler (upgraded to a Perkin Elmer 800 integrated system with Zeeman background correction for the 2003 samples). Samples from 1975 to 1998 inclusive were analyzed

for total Hg using cold vapor atomic absorption spectrophotometry (CVAAS) with the 3030b-AAS (Perkin-Elmer) equipped with VGA (Varian) vapor generation system and PSC-55 (Varian) autosampler. Samples collected in 2003 were homogenized, freeze-dried, homogenized again and weighed out directly into nickel combustion boats. Total Hg was analyzed using an Advanced Mercury Analyzer (AMA-254) equipped with an ASS-254 autosampler for solid samples according to CWS Method No. METCHEM-AA-03E (see also EPA Method 7473; Salvato and Pirola, 1996). The method employs direct combustion of the sample in an oxygen-rich atmosphere. Analytical accuracy for total Hg was determined by analyzing one or two blank samples with each sample set, as well as analysis of two standard reference materials (DOLT-2 and DORM-2 obtained from the Canadian National Research Council (CNRC)) for the 1975 to 1998 samples, and three standard reference materials (DOLT-2 and TORT-2 from CNRC and Oyster Tissue 1566b from the National Institute of Standards and Technology (NIST)) for the 2003 samples. Analytical accuracy for Se was determined by analyzing one or two blank samples with each sample set, as well as analysis of two standard reference materials (DOLT-2 and DORM-2 obtained CNRC). Analytical precision was checked by analyzing replicate samples for both Hg and Se. Recovery of reference materials was within the certified range for all methodologies and nominal detection limits were 0.04 mg g1 dry weight sample for total Hg (for both methods) and 0.4e0.5 mg g1 dry weight sample for Se.

2.4. Stable isotope analysis Dried egg homogenates were made available for stable nitrogen analysis following contaminant assays and so had already had lipids removed. Stable-nitrogen isotope assays were performed on 1 mg subsamples of homogenized materials by loading them into tin cups and combusting them at

B.M. Braune / Environmental Pollution 148 (2007) 599e613

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Table 2 Mean concentrations of organochlorines in eggs of black-legged kittiwakes (ng g1 wet weight  standard error) collected between 1975 and 2003 Year

1975

1976

1987

1993

1998

2003

n (no. pools) % Lipid

12 (4) 11.9  1.9

6 (2) 7.8

3 (1) 9.4

15 (5) 8.5  0.2

15 (5) 9.0  0.2

12 (4) 9.1  0.2

PnCB HCB SCBz a-HCH b-HCH SHCH cis-Chlordane trans-Nonachlor cis-Nonachlor Oxychlordane HE SCHLOR p,p0 -DDE SDDT OCS Dieldrin Mirex SMirex SPCB

3.2  0.4 75.0  8.9 80.1  9.4 1.2  0.1 2.8  0.3 4.0  0.4 0.6  0.06 3.4  0.3 1.9  0.2 41.6  7.2 10.7  1.4 58.1  8.9 243  43.5 243  43.5 1.4  0.4 14.3  0.8 7.4  1.2 15.1  2.4 1664  362

3.5 89.0 94.6 1.7 3.2 4.8 0.6 3.8 1.9 61.2 14.6 82.0 420 420 1.9 12.2 13.3 26.1 2869

2.2 32.7 36.4 1.2 2.5 3.6 0.6 4.6 0.3 25.4 7.6 38.5 108 108 0.7 8.8 4.0 8.6 511

1.4  0.2 23.7  1.8 26.5  2.0 1.9  0.2 2.9  0.3 5.0  0.5 0.2  0.08 3.7  0.5 1.7  0.1 20.2  1.9 7.6  1.0 33.4  2.4 70.5  4.8 70.5  4.8 0.6  0.04 7.5  1.0 4.1  0.4 9.5  1.3 330  51.5

2.2  0.3 25.3  3.5 29.1  4.1 1.1  0.2 4.1  0.7 5.2  0.8 0.5  0.05 3.3  0.3 2.1  0.1 17.8  1.0 7.9  1.0 31.7  2.0 60.2  8.0 60.2  8.0 0.6  0.08 9.2  0.2 3.4  0.3 7.3  1.1 280  22.4

1.0  0.05 15.7  0.9 17.9  1.0 1.3  0.2 6.4  0.5 7.7  0.6 0.5  0.02 2.2  0.1 1.2  0.1 34.5  3.3 6.8  0.4 45.3  3.7 43.5  6.5 43.5  6.5 0.3  0.02 5.3  0.3 2.1  0.3 4.6  0.6 177  26.0

Trend

p

R2adj

Y Y Y

<0.002 <0.00001 <0.00001 ns ns <0.05 <0.02 ns ns <0.0002 <0.006 <0.0003 <0.00001 <0.00001 <0.00001 <0.0002 <0.00002 <0.00007 <0.00001

0.56 0.85 0.83

[ Y

Y Y Y Y Y Y Y Y Y Y

0.27 0.44

0.51 0.33 0.48 0.85 0.85 0.76 0.66 0.68 0.61 0.86

Significantly increasing ([), decreasing (Y) or non-significant (ns, p > 0.05) time trends for organochlorine concentrations are indicated as determined by multiple linear regression analysis controlling for % lipid and d15N. The adjusted R2 is given for the whole model using year, % lipid and d15N as regressors. The number of eggs (n) is given with the number of egg pools shown in brackets. 1200  C in a Robo-Prep elemental analyzer. Resultant N2 gases were then analyzed using an interfaced Europa 20:20 continuous-flow isotope ratio mass spectrometer (CFIRMS) with every five unknowns separated by two laboratory standards. Stable nitrogen abundances were expressed in d notation as the deviation from standards in parts per thousand (&) according to the following equation:

dX ¼



  Rsample =Rstandard  1  1000

ð1Þ

where X is 15N and R is the corresponding ratio 15N/14N. The Rstandard values were based on atmospheric N2 (AIR). Replicate measurements of internal laboratory standards (albumen) indicate a measurement error of 0.3& for stable-nitrogen isotope measurements.

Table 3 Mean concentrations of organochlorines in eggs of northern fulmars (ng g1 wet weight  standard error) collected between 1975 and 2003 Year

1975

1976

1977

1987

1993

1998

2003

n (no. pools) % Lipid

15 (5) 11.41.1

12 (4) 11.6  2.2

15 (5) 9.0  0.6

6 (2) 9.9

15 (5) 11.7  1.0

15 (5) 11.3  0.4

15 (5) 10.5  0.4

PnCB HCB SCBz a-HCH b-HCH SHCH cis-Chlordane trans-Nonachlor cis-Nonachlor Oxychlordane HE SCHLOR p,p0 -DDE p,p0 -DDD p,p0 -DDT SDDT OCS Dieldrin Mirex SMirex SPCB

2.4  0.1 57.4  3.6 60.8  3.8 2.0  0.1 0.6  0.05 2.6  0.2 1.4  0.3 10.2  0.8 1.1  0.1 86.2  5.9 5.5  1.4 104  6.9 578  36.3 10.3  4.6 85.9  8.4 674  40.6 1.0  0.04 13.3  1.0 7.7  0.5 13.0  0.8 806  56.6

2.5  0.4 70.8  10.0 74.3  10.5 1.7  0.2 0.6  0.03 2.3  0.2 2.6  0.6 14.8  2.2 1.7  0.3 118  16.7 7.0  0.8 144  20.6 744  142 20.8  4.7 93.6  26.3 859  168 1.2  0.2 16.7  1.9 10.5  1.3 17.5  2.3 1017  178

2.1  0.3 45.8  3.7 48.7  3.9 1.7  0.2 0.3  0.20 2.0  0.4 1.8  0.2 10.0  0.7 1.3  0.1 74.1  5.5 4.7  0.4 91.9  6.4 371  51.0 5.2  2.7 49.0  3.2 425  52.0 1.0  0.1 10.7  1.1 6.6  0.5 11.6  0.8 606  46.4

2.0 30.1 32.7 1.4 0.8 2.2 1.7 12.8 1.7 64.7 5.2 86.2 202 6.0 10.2 218 0.5 10.6 4.8 9.1 338

2.2  0.2 50.5  3.6 53.6  3.9 1.7  0.3 1.1  0.3 3.1  0.7 1.9  0.3 19.4  2.8 1.9  0.3 92.8  15.8 11.4  1.5 128  17.5 365  21.7 1.3  0.2 29.4  2.5 396  23.6 1.2  0.1 17.4  1.6 8.6  0.7 17.7  1.5 510  36.1

1.5  0.1 32.8  3.8 35.0  4.0 0.6  0.08 0.8  0.14 1.5  0.2 1.7  0.1 19.8  3.0 2.8  0.4 64.9  5.9 6.6  0.9 95.9  9.8 192  19.9 2.4  0.3 14.4  2.7 209  22.2 1.0  0.3 13.9  1.4 6.4  0.5 12.9  1.0 267  20.0

0.5  0.09 13.2  1.0 14.0  1.0 1.6  0.2 4.2  0.6 5.7  0.7 0.9  0.07 7.9  0.6 0.9  0.08 97.1  6.8 4.5  0.3 112  7.6 112  11.3 1.0  0.2 10.9  1.4 124  12.7 0.4  0.04 6.9  0.6 3.7  0.3 7.1  0.5 167  15.5

Trend

p

R2adj

Y Y Y

<0.00001 <0.00001 <0.00001 ns <0.0005 <0.02 ns ns ns ns <0.05 ns <0.00001 <0.00002 <0.00001 <0.00001 ns ns <0.002 ns <0.00001

0.65 0.72 0.72

[ [

[ Y Y Y Y

Y Y

0.45 0.13

0.48 0.76 0.56 0.73 0.77

0.56 0.86

Significantly increasing ([), decreasing (Y) or non-significant (ns, p >0.5) time trends for organochlorine concentrations are indicated as determined by multiple linear regression analysis controlling for % lipid and d15N. The adjusted R2 is given for the whole model using year, % lipid and d15N as regressors. The number of eggs (n) is given with the number of egg pools shown in brackets.

0.70 Y

Y Y Y Y Y

Y

Significantly increasing ([), decreasing (Y) or non-significant (ns, p > 0.5) time trends for organochlorine concentrations are indicated as determined by multiple linear regression analysis controlling for % lipid and d15N. The adjusted R2 is given for the whole model using year, % lipid and d15N as regressors. The number of eggs (n) is given with the number of egg pools shown in brackets.

0.61 0.61 0.58 0.54 0.12

0.22

0.61 [

Y Y Y

1.9  0.1 27.6  1.1 31.9  1.4 3.4  0.1 7.8  0.5 11.2  0.5 0.5  0.07 0.5  0.14 2.9  0.4 22.4  0.7 4.1  0.4 30.5  1.6 103  8.0 103  8.0 0.7  0.02 9.1  0.9 1.4  0.9 3.0  1.2 120  22.4 3.2  0.3 47.2  5.0 53.7  5.7 11.6  0.9 7.3  1.0 20.0  2.1 0.5  0.08 0.4  0.10 4.4  0.8 13.6  1.4 5.3  0.6 24.2  2.7 139  20.6 139  20.6 1.7  0.2 12.9  1.9 1.2  0.2 3.0  0.4 148  20.1 4.4  0.5 111  16.3 118  17.4 5.7  0.9 3.4  0.6 9.2  1.3 0.7  0.14 0.4  0.03 4.8  0.8 13.2  1.9 3.5  0.5 22.5  3.0 197  8.3 197  8.2 2.1  0.2 14.3  2.5 1.6  0.2 3.0  0.4 248  2.0 PnCB HCB SCBz a-HCH b-HCH SHCH cis-Chlordane trans-Nonachlor cis-Nonachlor Oxychlordane HE SCHLOR p,p0 -DDE SDDT OCS Dieldrin Mirex SMirex SPCB

5.6  0.5 132  17.6 142  18.4 8.0  0.7 3.9  0.2 11.9  0.9 1.5  0.6 0.7  0.11 7.4  0.8 19.9  1.6 6.4  1.2 35.9  3.4 231  27.8 232  27.7 2.2  0.2 27.6  6.1 2.1  0.4 4.4  0.7 359  58.8

4.4  0.6 109  20.3 117  21.3 6.7  0.7 3.9  1.3 10.6  1.7 0.7  0.31 0.3  0.27 3.4  2.9 16.4  3.0 4.9  1.7 25.7  8.1 232  22.0 232  22.0 1.9  0.3 12.3  2.9 2.0  0.2 4.2  0.6 345  44.7

4.7  0.5 77.3  9.5 85.1  10.3 10.7  1.7 7.9  0.6 18.6  2.0 1.0  0.14 0.6  0.13 5.9  0.4 19.4  1.6 6.3  0.4 33.2  1.9 156  18.8 156  18.8 1.9  0.2 17.0  1.1 1.3  0.2 2.7  0.7 209  25.4

3.9  0.1 78.4  2.6 85.0  2.4 6.7  0.9 6.2  0.5 12.9  1.3 0.6  0.11 0.5  0.15 6.3  1.1 18.4  1.6 6.7  0.5 32.5  3.4 103  15.9 104  15.9 1.4  0.1 16.0  2.2 1.0  0.2 1.6  0.5 169  26.7

3.5  0.1 46.6  2.3 52.7  2.5 6.7  0.8 9.9  0.5 16.6  1.0 0.9  0.27 1.8  1.4 5.7  1.1 14.1  1.1 6.4  0.5 28.9  4.0 99.6  7.5 99.6  7.5 1.3  0.1 15.5  1.5 1.1  0.1 3.3  0.5 129  8.6

15 (5) 12.8  0.5 15 (5) 12.9  0.4 15 (5) 11.3  0.4 9 (3) 10.2  1.1 n (no. pools) % Lipid

9 (3) 12.4  1.2

9 (3) 11.7  0.4

9 (3) 11.4  0.9

9 (3) 10.8  0.5

1998 1993 1988 1987 1977 1976 1975 Year

Mean concentrations of organochlorines in eggs of thick-billed murres (ng g1 wet weight  standard error) collected between 1975 and 2003

Table 4

2003

Trend

p

<0.00001 <0.00001 <0.00001 ns <0.00001 ns <0.02 ns ns ns ns ns <0.00001 <0.00001 <0.00001 <0.0002 <0.03 ns <0.00001

R2adj

0.70 0.90 0.89

B.M. Braune / Environmental Pollution 148 (2007) 599e613

603

2.5. Statistical analysis All statistical tests were performed using Statistica for Windows Version 7.0 (StatSoft Inc., Tulsa, OK) with a significance level of p < 0.05. Only those compounds for which >90% of the samples had detectable concentrations for a given species were statistically analyzed. Non-detect values (<0.1 ng g 1) were set to one-half the detection limit for purposes of statistical analyses but not for calculation of the annual means which appear in Tables 2e4, or calculation of the sums of the major organochlorine groups (i.e. SPCB, SDDT, SCBz, etc.). Regression analyses indicated no significant relationship between % lipid and organochlorine contaminants for black-legged kittiwakes or thickbilled murres but a significant relationship was found for some compounds in the northern fulmars. Likewise, regression analyses also indicated significant relationships between d15N and some organochlorine compounds, which varied among the three species. Given this inconsistency in results, organochlorine data were analyzed for temporal trends by multiple regression analysis using year, % lipid and d15N as regressors. This method was used to account for variability in % lipid rather than lipid normalizing the data using the ratio approach (i.e. dividing contaminant concentration by lipid concentration) which could introduce greater error (Peakall and Gilman, 1979; Hebert and Keenleyside, 1995). Thus, organochlorine time trends could be evaluated while controlling for any variations in % lipid or trophic shifts in diet (as indicated by d15N). Likewise, total Hg and Se concentrations were analyzed for temporal trends by multiple regression analysis using year and d15N as regressors. Residuals from the regression analyses were tested for normality using the ShapiroeWilks’ W test and the concentration data loge-transformed if the residuals were found to violate the assumption of normality. Data on proportional contributions of individual compounds, isomers, metabolites and PCB homologs to chemical group totals were transformed using an arcsine transformation (Zar, 1984), as necessary, prior to linear regression analysis. The tabulated data are presented as arithmetic means in concentration units of ng g1 wet weight (ww) for the organochlorines and mg g1 dry weight (dw) for total Hg and Se. The Hg concentration data presented in the graphs have been adjusted for d15N according to the equation: Yadj ¼ Ymeasured þ A

h

d15 N

 average

i    d15 N measured

ð2Þ

where Y is the Hg concentration, A is the regression coefficient for d15N for each species, and the term [(d15N)average  (d15N)measured] calculates how much the measured d15N value differed from the d15N value averaged for each species over all years. The SPCB and SDDT concentration data presented in the graphs have been adjusted for d15N and % lipid according to the equation: i h    Yadj ¼ Ymeasured þ A d15 N average  d15 N measured i h þ B ð%lipidÞaverage ð%lipidÞmeasured

ð3Þ

where Y is the residue concentration, A is the regression coefficient for d15N and B is the regression coefficient for % lipid for each species, and the terms [(d15N)average  (d15N)measured] and [(% lipid)average  (% lipid)measured] calculate how much the measured d15N and % lipid values differed from the d15N and % lipid values averaged for each species over all years.

3. Results 3.1. Stable nitrogen Each species exhibited a range in mean d15N values among years indicating either trophic differences among cohorts of laying females or changes in baseline foodweb signature (Table 1). The greatest range in annual mean d15N values was observed in eggs of black-legged kittiwakes (14.1e 16.7&) while the least was observed in northern fulmar eggs (13.0e13.5&) while thick-billed murre eggs had an

B.M. Braune / Environmental Pollution 148 (2007) 599e613

intermediate range (14.8e15.8&) over all years of this study. Although linear regression of d15N values in eggs against year sampled indicated no significant temporal trends between 1975 and 2003 for any of the three species, analysis of variance (ANOVA) indicated that there were significant inter-year variations in d15N for all species (kittiwakes: p < 0.00001; fulmars: p < 0.01; murres: p < 0.02). Regression analyses also indicated significant relationships between d15N and some organochlorine compounds, which varied among the three species. Therefore, d15N was included as a regressor to control for these variations in the regression analyses used to examine changes in contaminant residues over time.

2.0 BLKI

1.5

μg g-1 dry wt.

604

1.0

0.5

2.0 NOFU

3.2. Mercury and selenium 1.5

μg g-1 dry wt.

Controlling for trophic variations in diet as represented by d15N, multiple regression analyses indicated significant increases in concentrations of total Hg in eggs of thick-billed murres and northern fulmars between 1975 and 2003 (Table 1, Fig. 2). With d15N held constant, Hg concentrations increased at an annual rate of 2.9% in thick-billed murres and 1.8% in northern fulmars during the 28 years of this study. Total Hg in eggs of black-legged kittiwakes did not change significantly over the study period. There was no significant temporal change in Se levels in any of the three species (Table 1).

1.0

0.5 Ln[Hg]=-37.7+0.018(Year)+0.117(δ15N) R2adj = 0.50, p < 0.0001

2.0 TBMU

3.3. Organochlorines 1.5

μg g-1 dry wt.

The primary organochlorines found in eggs of all three species were SPCB, SDDT (mainly p,p0 -DDE), SCBz (mainly HCB) and SCHLOR (mainly oxychlordane) (Tables 2e4). Controlling for % lipid and trophic variations in diet as represented by d15N, multiple regression analyses indicated that the majority of the organochlorine compounds analyzed showed either significant declines or no significant change between 1975 and 2003 in all three species (Tables 2e4). The exceptions to this were for heptachlor epoxide (HE) in northern fulmars, which appeared to be increasing due primarily to a single elevated mean value for 1993 (Table 3), and for significantly increasing concentrations of b-HCH in northern fulmars (Table 3) and thick-billed murres (Table 4), and SHCH in black-legged kittiwakes (Table 2) and northern fulmars (Table 3). The increasing SHCH concentrations in the northern fulmars were clearly being driven by b-HCH but the increasing SHCH levels in black-legged kittiwakes were also being driven by increasing b-HCH levels ( p ¼ 0.05). Concentrations of SPCB and SDDT (Fig. 3) as well as SCBz decreased significantly in eggs of all three species, whereas SCHLOR and SMirex decreased significantly in black-legged kittiwake eggs but not in the eggs of the other two species. SCBz was comprised mainly of hexachlorobenzene (HCB) in all three species although the mean proportional contribution of HCB to SCBz decreased significantly over time in the kittiwakes and the murres (Table 5). Concentrations of 1,2,3,4-tetrachlorobenzene and pentachlorobenzene (PnCB)

1.0

0.5 [Hg]=-51.3+0.026(Year)+0.077(δ15N) R2adj = 0.70, p < 0.00001

1975

1980

1985

1990

1995

2000

2005

1

Fig. 2. Mercury concentrations (mg g dry weight) in eggs of black-legged kittiwakes (BLKI), northern fulmars (NOFU) and thick-billed murres (TBMU) collected between 1975 and 2003. Each point represents the concentration for a pool of three eggs adjusted for d15N. Regression lines for significant changes based on adjusted data are also shown.

decreased significantly between 1975 and 2003, and levels of 1,2,4,5-tetrachlorobenzene remained unchanged in all three species. However, the mean proportional contributions of the tetra- and pentachlorobenzenes to SCBz all significantly increased over time except for PnCB in fulmars. SDDT was comprised almost entirely of p,p0 -DDE in the kittiwake and the murre eggs in all years (Table 5). In the fulmar eggs, p,p0 -DDE also predominated but at a lower proportion which significantly increased from 1975 to 2003 (Table 5) as the proportion of p,p0 -DDT progressively decreased. Although statistical analyses indicated a significant change in percent p,p0 -DDE in the eggs of thick-billed murres, as well,

B.M. Braune / Environmental Pollution 148 (2007) 599e613

BLKI

ng g-1 wet wt.

3000

Ln[ΣPCB]=191-0.094(Year)-0.052(%lipid)+0.102(δ15N) R2adj = 0.86, p < 0.00001 Ln[ΣDDT]=149-0.073(Year)-0.030(%lipid)+0.064(δ15N) 2 R adj = 0.85, p < 0.00001

2000

1000

1600 NOFU 15 Ln[ΣPCB]=106-0.049(Year)+0.093(%lipid)-0.338(δ N) 2 R adj = 0.86, p < 0.00001

ng g-1 wet wt.

1200

15 Ln[ΣDDT]=109-0.051(Year)+0.091(%lipid)-0.306(δ N) R2adj = 0.77, p < 0.00001

800

400

500 TBMU 15 [ΣPCB]=17669-8.94(Year)+22.0(%lipid)+4.15(δ N) R2adj = 0.70, p < 0.00001

ng g-1 wet wt.

400

[ΣDDT]=9942-4.89(Year)+6.81(%lipid)-9.03(δ15N) R2adj = 0.61, p < 0.00001

300

605

species to also show significant declines in photomirex and SMirex. The proportional contribution of mirex to SMirex changed only in the northern fulmars (Table 5) with a significant decrease in the mirex fraction and a concurrent significant increase in the photomirex fraction. The composition of SHCH differed among species. In the fulmars and murres, a-HCH was the predominant isomer in the mid-1970s, but progressively decreased as b-HCH increased in proportion (Table 5, Fig. 4). In kittiwakes, bHCH was the predominant isomer over the entire period of the study with an apparent increase since 1998 while the a-isomer was found in lesser proportions (Table 5, Fig. 4). In all species, g-HCH was largely not detected except in 1993, when it was detected in all species, and in 1998, when it was detected in the fulmar eggs only. Major PCB congeners found in the eggs, that is, those congeners averaging more than 5% of SPCB overall, included the following, in order of decreasing contribution, in kittiwakes: 153, 138, 180, 118 and 99; in fulmars: 153, 180, 138, 118 and 170/190; and in murres: 153, 138, 118, 187, 99 and 180. The penta-, hexa- and heptachlorobiphenyl homologs constituted the largest proportion of SPCB in all three species (Table 6). In the murres, however, the lower chlorinated biphenyls (tri- to pentachlorobiphenyls) constituted a larger proportion of SPCB than in the other two species (Table 6). Over time, however, there seems to have been a significant shift in the murres from the lower chlorinated biphenyls (tri- to pentachlorobiphenyls) to the higher chlorinated biphenyls (hexa- to octachlorobiphenyls). All three species showed an increase in the hexachlorobiphenyl fraction of SPCB over time (Table 6).

200

4. Discussion 100

4.1. Trophic level and migration 0 1975

1980

1985

1990

1995

2000

2005

Fig. 3. SPCB and SDDT concentrations (ng g1 wet weight) in eggs of blacklegged kittiwakes (BLKI), northern fulmars (NOFU) and thick-billed murres (TBMU) collected between 1975 and 2003. SPCB concentrations are shown as solid circles () and SDDT concentrations are shown as open circles (B). Each point represents the concentration for a pool of three eggs adjusted for d15N and % lipid. Regression lines based on adjusted data are also shown for SPCB (solid line) and SDDT (broken line).

these changes were comparatively minor given that the percent contribution of p,p0 -DDE to SDDT remained greater than 99.5% over all years. SCHLOR was made up of predominantly oxychlordane for all species, averaging 78% in northern fulmars, 66% in blacklegged kittiwakes and 60% in thick-billed murres. Heptachlor epoxide (HE), cis- and trans-nonachlor, and cis-chlordane were present in varying proportions. None of the individual chlordane-related compounds showed significant changes in proportional contributions to SCHLOR in any of the species over the period of this study. Mirex concentrations significantly decreased in eggs of all three species although black-legged kittiwakes were the only

Although d15N values in eggs indicated no significant temporal trends between 1975 and 2003 for any of the three species, there were significant inter-year variations in d15N which were particularly pronounced in the kittiwakes. Black-legged kittiwakes showed the greatest range in d15N values suggesting a more diverse diet than northern fulmars which showed the least variation in d15N values over the study period. However, based on d15N values measured in a variety of tissues, Hobson (1993) determined that black-legged kittiwakes, northern fulmars and thick-billed murres in Lancaster Sound overlapped significantly in trophic position. Similar findings were reported more recently for these three species in the North Water Polynya of northern Baffin Bay (Hobson et al., 2002). Kittiwakes feed at the surface; fulmars take their prey from the surface or during shallow dives; and thick-billed murres are pursuit divers, but all feed on fish, squid, amphipods and other crustacea in varying proportions, and northern fulmars will occasionally scavenge marine mammal carcasses (Baird, 1994; Gaston and Hipfner, 2000; Hatch and Nettleship, 1998). The d15N data from this study indicate that there was no consistent directional shift in trophic level which could

B.M. Braune / Environmental Pollution 148 (2007) 599e613

606

Table 5 Calculated proportions of DDE relative to SDDT, HCB to SCBz, HCH isomers to SHCH, and Mirex to SMirex in eggs of black-legged kittiwakes, northern fulmars and thick-billed murres collected between 1975 and 2003 p,p0 -DDE:SDDT

Species

Year

Black-legged kittiwake

1975 1976 1987 1993 1998 2003 Trend p R2adj

1.00 1.00 1.00 1.00 1.00 1.00

1975 1976 1977 1987 1993 1998 2003 Trend p R2adj

0.86 0.87 0.87 0.93 0.92 0.92 0.90

Northern fulmar

Thick-billed murre

1975 1976 1977 1987 1988 1993 1998 2003 Trend p R2adj

ns

HCB:SCBz 0.94 0.94 0.90 0.89 0.87 0.88 Y <0.00001 0.85 0.94 0.95 0.94 0.92 0.94 0.94 0.93

[ <0.00001 0.55 0.996 0.996 0.998 0.997 0.998 0.998 1.000 1.000 [ <0.00001 0.72

a-HCH:SHCH 0.30 0.34 0.32 0.38 0.23 0.17

0.70 0.66 0.68 0.57 0.77 0.83

Y <0.00001 0.64

0.94 0.93 0.94 0.91 0.92 0.88 0.88 0.87 Y <0.00001 0.86

Mirex:SMirex 0.50 0.51 0.47 0.44 0.53 0.45

Y <0.03 0.20 0.76 0.73 0.89 0.65 0.58 0.38 0.29

ns

b-HCH:SHCH

0.62 0.67 0.65 0.57 0.52 0.59 0.40 0.31 Y <0.00001 0.69

ns 0.24 0.27 0.11 0.35 0.36 0.54 0.71 [ <0.00001 0.72 0.38 0.33 0.35 0.43 0.48 0.36 0.60 0.69 [ <0.00001 0.59

ns 0.59 0.60 0.57 0.52 0.48 0.50 0.52 Y <0.00001 0.61 0.54 0.48 0.49 0.53 0.70 0.41 0.36 0.39 ns

Results ( p and adjusted R2) from linear regression analysis are also given (significantly increasing ([); significantly decreasing (Y); ns, not significant; p > 0.05). Sample sizes are indicated in Table 1.

explain temporal changes in the contaminant concentrations measured. All three species are migratory, dispersing to various areas throughout the North Atlantic for the winter. The kittiwakes likely overwinter on the Grand Banks off Newfoundland and possibly further south along the eastern seaboard of North America (Baird, 1994), whereas band return data suggest that the thick-billed murres from Prince Leopold Island overwinter in open waters off southwestern Greenland (Donaldson et al., 1997). There is evidence to suggest that northern fulmars from the Canadian Arctic may overwinter anywhere from the Labrador Sea to the Northeast Atlantic (Hatch and Nettleship, 1998; Mallory, 2005). These seasonal movements of the birds, which expose them to varying contaminant levels in the local prey species, were likely a contributing factor to the contaminant trends observed in this study. 4.2. Organochlorine trends The pattern of temporal decline reported here for most of the organochlorines in these migratory seabird species reflects overall lower contamination of the food chain both in the Arctic and in their oceanic wintering areas following restrictions

placed on the use of many of these compounds in the 1970s and 1980s in the United States, Canada and western European countries. Similar declines in most of the legacy persistent organic pollutants (e.g. PCBs, DDT) over recent decades have been documented for a number of seabird species throughout the marine environment of the northern hemisphere; e.g. gannets (Sula bassana) from western Scotland (Alcock et al., 2002), common terns (Sterna hirundo) from the Wadden Sea (Becker et al., 2001), guillemots/common murres (Uria aalge) and little terns (Sterna albifrons) from the Baltic Sea (Bignert et al., 1998; Thyen et al., 2000), six seabird species from the Barents Sea (Barrett et al., 1996), ´ lafsdo´ttir black guillemots (Cepphus grylle) from Iceland (O et al., 2005), common and thick-billed murres from Alaska (Vander Pol et al., 2004), and double-crested (Phalacrocorax auritus) and pelagic (P. pelagicus) cormorants from the west coast of Canada (Harris et al., 2005), as well as for other marine biota from the Canadian Arctic such as ringed seals (Phoca hispida), beluga (Delphinapterus leucas) and polar bears (Ursus maritimus) (Braune et al., 2005). The black-legged kittiwake showed a significant decrease in the greatest number of organochlorine compounds (Table 2) compared with the other two arctic species (Tables 3 and 4)

B.M. Braune / Environmental Pollution 148 (2007) 599e613 100 BLKI 80

60

40

20

100 NOFU

Percent of ΣHCH

80

60

40

20

100 TBMU 80

60

40

20

0 1975

1980

1985

1990

1995

2000

2005

Fig. 4. Mean percent contribution of a-HCH (diagonal-hatched bar), b-HCH (black bar), and g-HCH (cross-hatched bar) to SHCH in eggs of black-legged kittiwakes (BLKI), northern fulmars (NOFU) and thick-billed murres (TBMU) collected between 1975 and 1998.

in this study. This pattern is likely attributable primarily to exposure differences in overwintering areas. Kittiwakes overwinter at lower latitudes than the other two species, placing them closer to historical sources of many of the compounds, which would have resulted in greater exposure to those contaminants during the 1970s and a faster rate of decline following reductions in their use. For example, assuming % lipid and d15N are held constant, SPCB in kittiwake eggs decreased at an annual rate of 8.9% compared with 4.7% and 4.2% in eggs of fulmars and murres, respectively, between 1975 and 2003. Likewise, SDDT in kittiwake eggs decreased at an annual rate of 7.1% compared with 4.9% and 3.2% in eggs of fulmars and murres, respectively. Hepatic concentrations of SPCB and SDDT measured by Buckman et al. (2004) in

607

these same three species from northern Baffin Bay in 1998 found that fulmars had the highest concentrations and murres, the lowest. Our data for eggs from 1998, show that the fulmars had higher concentrations of SDDT than the other two species but SPCB was highest in the kittiwakes followed closely by the fulmars. In northern fulmars, concentrations of p,p0 -DDT were measurably higher in the 1970s than in recent samples (Table 3). A significant proportional shift occurred in the fulmars from p,p0 DDT to p,p0 -DDE over the period of this study (Table 5) suggesting greater exposure to DDT in the 1970s than for the other two species. The greater exposure of fulmars to DDT compared with the other two species could have been associated with the possibility of fulmars overwintering in the northeast Atlantic which would have brought them closer to sources of continued DDT use in Russia and other eastern European countries during the 1970s and 1980s, well after the ban on DDT use went into effect in the US, Canada and most western European countries in the early 1970s (AMAP, 2004). There was a significant shift in PCBs from the lower chlorinated biphenyls to the hexachlorobiphenyls in all three species (Table 6) suggesting that the lower chlorinated congeners were declining faster than the higher chlorinated congeners. This pattern has also been observed in gannet eggs from Scotland (Alcock et al., 2002) and in herring gull (Larus argentatus) eggs from the Great Lakes (Hebert et al., 1999a). Half-lives of PCBs in eggs have been shown to generally increase with increasing degree of chlorination, reflecting the greater environmental persistence of congeners with higher log Kow values (Alcock et al., 2002; Drouillard et al., 2001). In conjunction with this gradation in clearance potential at the biological level, one must also take into consideration the compound’s Arctic contamination potential (ACP) which is a function of its partitioning properties between air, water and n-octanol, and determines a chemical’s global transport pathway and its potential for bioaccumulation (Wania, 2003). Wania (2006) demonstrated that PCBs with an intermediate degree of chlorination (e.g. hexachlorobiphenyls) have a higher ACP than either light or heavy congeners. The significant declines in SCBz observed in all three species reflects the continued declining use of chlorobenzenes, in general, and HCB, in particular (AMAP, 2004; Bailey, 2001). Wania (2006) determined that HCB has a very high ACP value due to its high persistence in air and surface media and its partitioning characteristics. In our study, eggs of thick-billed murres had the highest concentrations of HCB compared with fulmars and kittiwakes throughout the study period which may reflect the length of time these birds spend at higher latitudes. However, Buckman et al. (2004) found that, of those three species sampled from northern Baffin Bay in 1998, northern fulmars had the highest mean hepatic concentration of HCB and thick-billed murres, the lowest. This difference may reflect differences in overwintering areas for the various murre populations breeding in the Canadian Arctic (Donaldson et al., 1997). Proportions of the tetra- and pentachlorobenzenes significantly increased, and those of HCB significantly decreased, over the study period in both the kittiwakes and

B.M. Braune / Environmental Pollution 148 (2007) 599e613

608

Table 6 Calculated proportions of PCB homologs relative to SPCB in eggs of black-legged kittiwakes, northern fulmars and thick-billed murres collected between 1975 and 2003 Species

Year

Tri

Tetra

Penta

Hexa

Black-legged kittiwake

1975 1976 1987 1993 1998 2003 Trend p R2adj

<0.01 <0.01 <0.01 <0.01 <0.01 <0.01

0.08 0.07 0.05 0.05 0.05 0.06 Y <0.001 0.44

0.19 0.20 0.17 0.16 0.17 0.16 Y <0.01 0.31

0.43 0.44 0.46 0.47 0.48 0.48 [ <0.00001 0.71

0.21 0.21 0.23 0.23 0.21 0.23

0.06 0.05 0.05 0.06 0.06 0.06

ns

ns

ns

1975 1976 1977 1987 1993 1998 2003 Trend p R2adj

<0.01 <0.01 <0.01 <0.01 <0.01 <0.01 <0.01

0.06 0.05 0.05 0.05 0.04 0.05 0.04 Y <0.0001 0.39

0.18 0.18 0.18 0.19 0.17 0.19 0.18

0.42 0.43 0.42 0.44 0.46 0.48 0.47 [ <0.00001 0.81

0.23 0.24 0.24 0.24 0.24 0.21 0.23 Y <0.04 0.11

0.07 0.07 0.07 0.06 0.06 0.04 0.07 Y <0.04 0.11

0.03 0.03 0.03 0.01 0.02 0.02 0.01 Y <0.00001 0.56

1975 1976 1977 1987 1988 1993 1998 2003 Trend p R2adj

0.02 0.03 0.02 0.02 0.02 0.01 0.02 0.02 Y <0.01 0.22

0.12 0.17 0.10 0.09 0.11 0.08 0.09 0.08 Y <0.001 0.33

0.24 0.24 0.22 0.23 0.25 0.21 0.22 0.19 Y <0.001 0.37

0.37 0.34 0.40 0.42 0.39 0.43 0.41 0.42 [ <0.002 0.30

0.19 0.17 0.19 0.19 0.19 0.21 0.20 0.21 [ <0.02 0.16

0.05 0.05 0.06 0.04 0.04 0.05 0.05 0.08 [ <0.02 0.15

<0.01 <0.01 0.01 <0.01 <0.01 <0.01 0.02 <0.01

Northern fulmar

Thick-billed murre

ns

ns

ns

Hepta

Octa

Nona 0.02 0.02 0.02 0.02 0.03 <0.01

ns

Results ( p and adjusted R2) from linear regression analysis are also given (significantly increasing ([); significantly decreasing (Y); ns, not significant, p > 0.05). Sample sizes are indicated in Table 1.

the murres which may reflect a biotransformation of HCB to the lower chlorinated tetra- and pentachlorobenzenes as described by Renner (1988). However, relative proportions of HCB and PnCB remained unchanged in the fulmars suggesting either a different metabolic capacity in this species or a continued low level exposure to HCB. Such exposure may occur on the overwintering grounds of the fulmars in the northeast Atlantic which are not far from Russia and other countries bordering the Baltic Sea which still emit quantities of HCB (AMAP, 2004). Although OCS is regarded as persistent and highly bioaccumulative (AMAP, 2004), concentrations of OCS were relatively low in eggs of all three seabird species. Magnesium production and chlorine manufacturing were historically important sources of OCS (AMAP, 2004). North American emissions of OCS in the 1960s probably resulted from the disposal of wastes associated with the chlorine manufacturing process using graphite electrodes, a process which was discontinued in the 1970s (AMAP, 2004). The significant declines of OCS observed in both the kittiwakes and the murres probably reflects this change in emissions. Mirex, historically used as an insecticide and a fire retardant, is an extremely persistent and relatively volatile

compound capable of undergoing long-range transport (AMAP, 1998). Mirex is photolytically degraded to photomirex, and both compounds are resistant to biodegradation (Norstrom et al., 1980). Mirex concentrations significantly decreased in eggs of all three species although black-legged kittiwakes were the only species to also show significant declines in photomirex and SMirex. The proportional contribution of mirex to SMirex changed only in the northern fulmars with a significant decrease in the mirex fraction and a concurrent significant increase in the photomirex fraction. Mirex is no longer produced (AMAP, 2004). Therefore, bearing in mind that the murres and fulmars spend more time in northern latitudes than do the kittiwakes, the fact that concentrations of photomirex in eggs of the fulmars and murres did not change over the study period and that the proportion of photomirex actually increased in the fulmars suggests that the mirex transported to northern latitudes has been photolytically degraded to photomirex and/or that photomirex is more persistent than mirex. Dieldrin concentrations significantly decreased in the eggs of the kittiwakes and murres but not in the fulmars. Dieldrin was used mainly as a soil insecticide but world production ceased in 1991 (AMAP, 2004). It would be expected that

B.M. Braune / Environmental Pollution 148 (2007) 599e613

decreasing concentrations of dieldrin would be reflected in the fulmar eggs, as well, over future sampling years. SCHLOR concentrations decreased significantly only in the kittiwake eggs even though the highest concentrations were consistently measured in the fulmar eggs. Buckman et al. (2004) also found that hepatic SCHLOR concentrations were highest in the fulmars from northern Baffin Bay compared with kittiwakes and murres. The lack of change in concentrations of oxychlordane and trans-nonachlor in the murres and fulmars between 1975 and 2003 (Tables 3 and 4) is con´ lafsdo´ttir et al. (2005) for black sistent with the findings of O guillemots from Iceland over a similar time period (1976e 1996). Although chlordane use patterns were restricted in the 1980s and finally banned worldwide in 1997 (AMAP, 2004), chlordane is persistent in the environment and some chlordane compounds (i.e. cis- and trans-chlordane), in particular, are highly volatile (AMAP, 1998) facilitating atmospheric transport to the Arctic. The change in chlordane concentrations in the kittiwakes probably reflects the change in chlordane use patterns near the overwintering areas of kittiwakes in more temperate latitudes. Oxychlordane was the major chlordane metabolite found in the eggs of all three seabird species and proportional contributions to SCHLOR did not change over the study period. Fulmars averaged the highest percent (78%) of oxychlordane and murres, the lowest, which compares favorably with the findings of Fisk et al. (2001) for these species. Those authors suggested that thickbilled murres have a higher capacity to metabolize and eliminate chlordane compared with other seabird species. The only organochlorines which increased significantly in all three species were b-HCH in the fulmars and murres (Tables 3 and 4), and SHCH in the kittiwakes and fulmars (Tables 2 and 3). The increasing SHCH concentrations in the black-legged kittiwakes, however, were also due to increasing b-HCH levels. The increasing concentrations of bHCH are consistent with the recalcitrant nature of this isomer as reflected by the increasing proportions of b-HCH found in the seabird eggs over time (Table 5, Fig. 4) as well as in other marine animals such as ringed seals and polar bears (Braune et al., 2005). HCH isomers are subject to biotransformation, and seabirds appear to readily metabolize the g and a isomers whereas b-HCH biomagnifies in the food web (Borga˚ et al., 2004; Hop et al., 2002; Moisey et al., 2001). This is consistent ´ lafsdo´ttir et al. (2005) who showed that with the findings of O levels of a-HCH declined much faster than b-HCH in immature black guillemots from Iceland between 1976 and 1996, a difference which may have been due to both biotransformation and exposure. Decreasing HCH concentrations were also found for a number of seabird species from the Barents Sea (Barrett et al., 1996). The differences in trends may be related to the spatial patterns found for HCHs in Arctic Ocean surface waters which indicate that concentrations are highest in the Beaufort Sea and Canadian Archipelago, intermediate in the Bering-Chukchi Seas, and lowest in the Barents Sea and eastern Arctic Ocean (Macdonald et al., 2000). HCHs are the most abundant pesticides in arctic air and water (Macdonald et al., 2000). Historically, HCH was released

609

into the environment in two forms; as technical HCH, which was comprised of eight isomers, the three main ones being aHCH (60e70%), b-HCH (5e12%) and g-HCH (10e12%), and as lindane, which consists almost entirely of g-HCH, the insecticidal form (Li and Macdonald, 2005). Although technical HCH is no longer used, many countries continue to use lindane. Air concentrations of a-HCH responded rapidly to reductions in global HCH use, particularly by China, India and other Asian countries, whereas atmospheric data for bHCH do not reflect the global emission patterns (Li and Macdonald, 2005). The difference in response is due to the fact that b-HCH partitions more strongly into water than does a-HCH (Li and Macdonald, 2005). Therefore, most of the bHCH was deposited into the North Pacific Ocean through precipitation and air-sea exchange before the air masses even reached the Arctic. Since transport by water is a much slower route compared with atmospheric transport, there has been a delay of about 10 years in the arrival of b-HCH to the Arctic via ocean currents through the Bering Strait. The difference in delivery patterns between these two HCH isomers is reflected in the biota. Calculated a-HCH:b-HCH ratios for murre eggs collected in 1999 from Little Diomede Island in the Bering Strait, St. George Island in the Pribilof Island chain and St. Lazaria Island off the southwestern coast of Alaska were at least 10 times lower than the ratio calculated for murre eggs collected from Prince Leopold Island in 1998 (Table 7), illustrating the higher proportion of b-HCH in waters entering the Arctic Ocean through the Bering Strait compared with the Canadian Arctic archipelago. Likewise, calculated a-HCH:b-HCH ratios in subcutaneous fat for two species of albatross collected from Southwest Midway Atoll in the North Pacific Ocean during 1997/1998 were at least 40 times lower than the ratio calculated for northern fulmars, which are related to albatrosses, collected from northern Baffin Bay in 1998 (Table 7). 4.3. Mercury trends A significant portion of global atmospheric Hg is estimated to come from anthropogenic sources (Macdonald et al., 2000) and, despite recent declines in anthropogenic emissions of Hg from Europe and North America, Hg emissions may be increasing globally (Pacyna and Pacyna, 2002). Although no significant changes in arctic atmospheric Hg concentrations have been recorded in recent years (Steffen et al., 2005), fluxes of Hg to the Arctic have increased (Macdonald et al., 2005). Mercury concentrations in marine biota from the Canadian Arctic are substantially higher than elsewhere in the Arctic, and increases in concentrations over the past few decades have been documented for a number of Canadian Arctic species (Braune et al., 2005) including two species of seabirds from this study (Fig. 2). Mercury concentrations have also increased in ringed seals from nearby northwestern Greenland (Riget et al., 2004). This is in contrast to time series data showing no change or decreasing Hg concentrations in seabirds at lower latitudes such as herring gulls from the Great Lakes (Koster et al., 1996), common terns from the New Jersey coast

B.M. Braune / Environmental Pollution 148 (2007) 599e613

610

Table 7 Calculated ratios of a-HCH:b-HCH in seabirds from the North Pacific, Alaska and the Canadian Arctic, 1997e1999 Tissue and species

Location

Year

Egg Murre (Uria spp.) Common murre (Uria aalge) Common murre (Uria aalge) Thick-billed murre (Uria lomvia) Northern fulmar (Fulmarus glacialis) Black-legged kittiwake (Rissa tridactyla)

Little Diomede I (Bering Strait) St. George I (Bering Sea) St. Lazaria I (NE Pacific) Prince Leopold I Prince Leopold I Prince Leopold I

1999 1999 1999 1998 1998 1998

Subcutaneous fat Black-footed albatross (Diomeda nigripes) Laysan albatross (Diomeda immutabilis) Northern fulmar (Fulmarus glacialis) Thick-billed murre (Uria lomvia) Black-legged kittiwake (Rissa tridactyla)

SW Midway Atoll (North Pacific) SW Midway Atoll (North Pacific) Northern Baffin Bay Northern Baffin Bay Northern Baffin Bay

1997/1998 1997/1998 1998 1998 1998

a

a-HCH:b-HCH 0.05 0.07 0.07 0.69 0.72 0.31 <0.01 0.01 0.48 0.32 0.19

Ref.a 1 1 1 This study This study This study 2 2 3 3 3

Ratios of a-HCH:b-HCH were calculated based on data presented in: (1) Vander Pol et al. (2004); (2) Guruge et al. (2001); (3) Buckman et al. (2004).

(Burger and Gochfeld, 2004) and the Wadden Sea (Becker et al., 2001), and little terns from the Baltic Sea (Thyen et al., 2000). Mercury concentrations in thick-billed murre eggs from Prince Leopold Island (1993, 0.30  0.05 mg g1 ww; 1998, 0.33  0.05 mg g1 ww; 2003, 0.37  0.08 mg g1 ww) were several times higher than comparable Hg concentrations in thick-billed murre eggs from colonies in Alaska (2000/2001, 0.04e0.10 mg g1 ww; Day et al., 2006) and northern Norway (1992/1993, 0.07e0.20 mg g1 ww; Barrett et al., 1996). Mercury concentration in eggs of black-legged kittiwakes from the Canadian Arctic (1993, 0.14  0.02 mg g1 ww), however, were very similar to Hg concentrations in kittiwake eggs from several locations in northern Norway from the same time period (1992/1993, 0.13 mg g1 ww; Barrett et al., 1996). Concentrations of total Hg measured by Campbell et al. (2005) in muscle and liver of these same three species from northern Baffin Bay in 1998 found that fulmars had the highest concentration and kittiwakes, the lowest, which matches our findings for Hg in eggs collected in 1998. Atwell et al. (1998), however, found just the opposite; kittiwakes had the highest total Hg and fulmars, the lowest, in muscle of these three species collected from Lancaster Sound in 1988e1990. It should, however, be noted that Hg accumulates more readily in liver than in muscle and, therefore, liver may be a better indicator of exposure. Based on a comparison of annual rates of change, Hg concentrations increased 60% more rapidly in eggs of thick-billed murres than in northern fulmars from Prince Leopold Island during the 28 years of this study whereas Hg in eggs of black-legged kittiwakes did not change significantly over the study period. Since the kittiwakes overwinter at lower latitudes than the other two species, their exposure to Hg is probably less for at least part of the year, given that North American emissions of Hg have decreased. The murres and fulmars, however, overwinter at higher latitudes in the North Atlantic which may contribute to their greater exposure to Hg year-round. The difference in annual rates of increase between the murres and the fulmars may be related to differences in Hg exposure from prey consumed in the different overwintering areas.

4.4. Toxicological significance Concentrations of total Hg, Se and organochlorine compounds in eggs collected from Prince Leopold Island between 1975 and 2003 were below toxicological threshold levels for eggs of wild birds (see reviews by Blus, 1996, 2003; Heinz, 1996; Hoffman et al., 1996; Ohlendorf, 2003; Peakall, 1996; Rice et al., 2003; Thompson, 1996; Wiemeyer, 1996; Wiener et al., 2003; Wolfe et al., 1998). Since most of the contaminants measured in this study were either decreasing or not showing much change over time, those concentrations are not currently of toxicological concern. Concentrations of total Hg in eggs of northern fulmars and thick-billed murres, as well as SHCH and/or b-HCH levels in all three species, however, were increasing. Mercury is an extremely potent embryo toxicant, and dietary Hg is rapidly transferred to avian eggs on a dose-dependent basis, making reproduction one of the most sensitive endpoints of Hg toxicity (Wolfe et al., 1998). The most bioavailable and toxic form of Hg is methylmercury and nearly 100% of the Hg transferred to eggs is methylmercury (Wiener et al., 2003). Based on a review of the literature, it has been suggested that concentrations of 0.5e2.0 mg g1 ww of Hg in eggs are sufficient to induce impaired reproductive success in a variety of bird species (Thompson, 1996). Although our levels are well below the published threshold values, Hg concentrations in the murre and fulmar eggs were increasing, suggesting that monitoring should be maintained to detect any future changes. Studies measuring levels of HCH in eggs have not found any associated toxic effects (Wiemeyer, 1996) and our data are about three orders of magnitude below those reported levels. However, b-HCH is thought to have estrogenic effects (Willett et al., 1998) and therefore, given the increase in concentrations of b-HCH observed, continued monitoring of HCHs is warranted. 5. Conclusions Concentrations of total Hg increased significantly in eggs of thick-billed murres and northern fulmars between 1975 and 2003 whereas Hg in eggs of black-legged kittiwakes did

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not change significantly over the study period. The primary organochlorines found in eggs of all three species were SPCB, p,p0 -DDE, oxychlordane, and HCB. The majority of organochlorines analyzed showed either significant declines or no significant change over the study period. However, significant increases were observed for SHCH in the kittiwakes and fulmars, and b-HCH in the murres and fulmars. Proportionally, b-HCH was the predominant isomer in the kittiwakes over the entire study period whereas in the fulmars and murres, a-HCH was the predominant isomer in the mid-1970s, but progressively decreased as b-HCH increased in proportion. There were significant shifts in the PCB congener pattern over time with an increase in the hexachlorobiphenyl fraction of SPCB in all three species. The seasonal movements of the birds, exposing them to changing contaminant patterns in both their summer and winter ranges, in conjunction with the biotransformation/biomagnification potential of the various compounds, best explain the observed trends of contaminant exposure in these species. Although the contaminant concentrations reported in this study are well below published threshold values, Hg and b-HCH concentrations continue to increase. Therefore, monitoring should be maintained to detect any future changes. Acknowledgements Thanks to David Nettleship, Tony Gaston and all of the field crews for their collection of the seabird eggs over the years. In particular, I thank Ilya Storm, Garry Donaldson and Kerry Woo, whose climbing skills and Arctic experience were essential for the more recent egg collections. Sample preparation and chemical analyses for contaminants were carried out by the Laboratory Services personnel at the National Wildlife Research Centre. Ewa Neugebauer, Henry Won and Michael Mulvihill carried out the chemical analyses. Stablenitrogen isotope analyses were coordinated by Keith Hobson of Environment Canada in Saskatoon with isotopic measurements carried out at the Department of Soil Science, University of Saskatchewan. I am also extremely grateful to Brian Collins for his advice on statistical analyses. Funding was provided by Environment Canada and the Northern Contaminants Program of Indian and Northern Affairs Canada. Logistical support out of Resolute Bay was provided by the Polar Continental Shelf Project, Natural Resources Canada. Comments from Craig Hebert, Brian Collins and two anonymous reviewers on earlier drafts of this manuscript were greatly appreciated. References Alcock, R.E., Boumphrey, R., Malcolm, H.M., Osborn, D., Jones, K.C., 2002. Temporal and spatial trends of PCB congeners in UK gannets. Ambio 31, 202e206. AMAP, 1998. AMAP Assessment Report: Arctic Pollution Issues. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway. AMAP, 2004. AMAP Assessment 2002: Persistent Organic Pollutants in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway.

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