Marine Pollution Bulletin xxx (2015) xxx–xxx
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Mercury concentrations in feathers of marine birds in Arctic Canada Mark L. Mallory a,⇑, Birgit M. Braune b, Jennifer F. Provencher c, D. Benjamin Callaghan a, H. Grant Gilchrist b, Samuel T. Edmonds d,1, Karel Allard e, Nelson J. O’Driscoll d a
Department of Biology, Acadia University, 15 University Drive, Wolfville, Nova Scotia B4P 2R6, Canada National Wildlife Research Centre, Environment Canada, Raven Road, Carleton University, Ottawa, Ontario K1A 0H3, Canada c Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1A 0H3, Canada d Department of Earth and Environmental Science, Acadia University, 15 University Drive, Wolfville, Nova Scotia B4P 2R6, Canada e Environment Canada, 17 Waterfowl Lane, Sackville, New Brunswick E4L 1G6, Canada b
a r t i c l e
i n f o
Article history: Received 27 April 2015 Revised 22 June 2015 Accepted 25 June 2015 Available online xxxx Keywords: Arctic Marine bird Mercury Ivory gull Photodemethylation
a b s t r a c t Mercury (Hg) concentrations are a concern in the Canadian Arctic, because they are relatively high compared to background levels and to similar species farther south, and are increasing in many wildlife species. Among marine birds breeding in the Canadian Arctic, Hg concentrations have been monitored regularly in eggs and intermittently in livers, but feathers have generally not been used as an indicator of Hg exposure or burden. We examined Hg concentrations in six marine bird species in the Canadian Arctic. Ivory gull Pagophila eburnea, feather Hg was exceptionally high, while glaucous gull Larus hyperboreus feather Hg was unexpectedly low, and ratios of feather THg to egg THg varied across species. The proportion of total Hg that was comprised of methyl Hg in ivory gull feathers was lower than in other species, and may be related to photo-demethylation or keratin breakdown in semi-opaque feather tissue. Ó 2015 Elsevier Ltd. All rights reserved.
Mercury (Hg) concentrations are elevated in many ecosystems across the Canadian Arctic (Dietz et al., 2013; Lavoie et al., 2013). Different forms of mercury (species) occur in the environment, with methylmercury (MeHg) readily accumulating in organisms due to its affinity for cellular proteins (Dietz et al., 2013), and thereby accounting for the majority of the mercury found within tissues in higher trophic levels of a system (>90%; Ackerman et al., 2013), compared to inorganic mercury species. MeHg may be detrimental to organisms because it has negative impacts on their physiology, including acting as a neurotoxin and immunotoxin (Wolfe et al., 1998). Methylmercury will biomagnify in food webs by a factor of 4–10 per trophic step (Kidd et al., 2011; Lavoie et al., 2013). Hence, organisms feeding at high trophic levels may accrue high concentrations of MeHg. This is particularly evident in Arctic marine birds (Braune et al., 2002, 2006, 2014). To date, most Hg research on marine birds in the Canadian Arctic has examined concentrations in liver, muscle or egg tissues (Mallory and Braune, 2012). However, for most seabirds in the Canadian Arctic, sampling Hg in feathers has not been undertaken to date, despite the advantages that the bird or egg does not need to be destroyed during sampling (a particular benefit in the case of
⇑ Corresponding author. 1
E-mail address: [email protected] (M.L. Mallory). Current address: TRC, Inc, 14 Gabriel Dr, Augusta, ME 04330, USA.
rare species), shed feathers may be taken from nests, and that feathers are chemically stable (i.e., Hg concentrations do not change in feathers once they are grown; Appelquist et al., 1984). Concentrations of Hg in feathers can vary markedly depending on sex, age and molt sequence (Braune and Gaskin, 1987; Bond and Diamond, 2009), and therefore knowledge of species molt patterns and chronology is essential for interpreting Hg concentrations from feathers. Despite variation among feathers and feather groups, feather sampling has enabled determination of Hg load in certain marine bird species (reviewed in Burger, 1993), including for example northern fulmar Fulmarus glacialis (Thompson et al., 1992a,b), Bonaparte’s gull Larus philadelphia (Braune and Gaskin, 1987), herring gull Larus argentatus (Thompson et al., 1993), and albatrosses (Tavares et al., 2013). Recently, Bond et al. (2015) found a disconcerting pattern in MeHg in feathers from one Arctic seabird, the ivory gull (Pagophila eburnea), an endangered species in Canada. Using breast feathers from museum specimens, they measured a 45-fold increase in MeHg in ivory gull feathers over the period 1877– 2007, and argued that Hg loads may have contributed to the decline of this species in the past three decades (Gilchrist and Mallory, 2005). We conducted a pilot study to assess Hg variation in primary feathers across marine bird species breeding in Arctic Canada, to establish reference values for these birds, and in particular for
http://dx.doi.org/10.1016/j.marpolbul.2015.06.043 0025-326X/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Mallory, M.L., et al. Mercury concentrations in feathers of marine birds in Arctic Canada. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.043
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two of the key gull species identified by Provencher et al. (2014) for concern with Hg levels, ivory gull and glaucous gull (Larus hyperboreus). If concentrations of Hg in feathers varied according to the known trophic position of each species (as they vary in eggs and livers; Provencher et al., 2014), then we predicted that: (1) across bird species, total mercury (THg) and methylmercury (MeHg) concentrations in feathers would be higher in birds occupying higher trophic positions; and (2) mercury concentrations found in feathers would be correlated with those in the literature for mercury concentrations in eggs. Feather samples of six species of Canadian Arctic-breeding marine birds were collected from 2009 to 2011 from four locations in the Canadian Arctic (Nunavut Territory; Fig. 1), the same locations where eggs have been monitored for Hg (Braune et al., 2006; Akearok et al., 2010). While the ivory gull remains in Arctic waters year-round (Spencer et al., 2014), the other bird species likely spend the winter south of the Arctic in coastal and offshore waters of the northwest Atlantic Ocean (Mosbech et al., 2006; Mallory et al., 2008a; Gaston et al., 2011; Frederiksen et al., 2012). We wanted to compare Hg concentrations in feathers that had been grown by marine birds while in the Arctic, and presumably when relying on foods acquired in the Arctic to supply much of the nutrients for feather growth (although some Hg would reflect longer-term concentrations in the body from year-round exposure). Consequently, we referred to published guides reporting the known feather molt patterns of these species (Ginn and Melville, 1983; Gaston and Hipfner, 2000; Goudie et al., 2000; Mallory et al., 2008b, 2012a,b; Weiser and Gilchrist, 2012) to select feathers grown while the birds were in the Arctic. For all species, this meant analyzing one of their inner primary (flight) feathers, which would have been among those grown during or shortly after the previous breeding season prior to southward migration. However, for the ivory gull, a species that spends its entire year in Arctic waters, we also analyzed some body and tertial feathers, as the collection of feathers from nests was opportunistic. Because Hg content can vary with feather position and molt sequence (Braune, 1987; Head et al., 2011), we standardized to the extent possible by sampling the same feathers within and across species. Primary feathers (position 1, 2 or 3) were collected for analysis from carcasses of thick-billed murre (Uria lomvia; n = 10), northern fulmar (n = 10), and black-legged kittiwake (Rissa tridactyla; n = 2) at Prince Leopold Island (74°N, 90°W) in 2009 as part of an International Polar Year project (Gaston et al., 2011). Shed feathers of ivory gull (P. eburnea; n = 8) were collected in 2010 from eight different nests on Seymour Island (Mallory et al., 2012a); these were mostly primary feathers (estimated positions 2–5), although some body feathers and tertials were collected. Primary feathers (position 2, 3 of three birds, position 4, 5 of one bird) of glaucous gull (L. hyperboreus; n = 4) were sampled in 2010 from carcasses collected from Nasaruvaalik Island (75.8°N, 96.3°W) as part of a long-term study at that site (Mallory et al., 2012b). Primary feathers (position 1, 2 or 3) of common eider (Somateria mollissima borealis; n = 10) were collected in 2011 from carcasses of birds sampled near Cape Dorset (64.2°N, 76.6°W; Provencher, 2013). We analyzed THg from the third primary and MeHg from the second primary, with the exception of the one glaucous gull (above) and ivory gull feathers. Sample feathers were cleaned for analysis by washing three times with Milli-Q water and were then oven-dried overnight at 60 °C. The weight of the dry feathers was measured to the nearest 0.1 mg and recorded. Those feathers weighing 650 mg were digested in 10 mL of 25% KOH/MeOH solution, while those >50 mg were digested in 40 mL of 25% KOH/MeOH solution. A sample aliquot (20 lL) of the digested sample was transferred to a reaction bubbler and analyzed for MeHg and inorganic Hg content through ethylation with NaB(C2H5)4 and purge-and-trap gas
chromatography prior to detection by atomic fluorescence spectroscopy (Brooks Rand Model III) by Florida Department of Environmental Protection method HG-003-2.10 (Edmonds et al., 2012). Concurrent calibration for MeHg and Hg(II) was performed and THg was determined by addition of inorganic and methylmercury values. Internal quality control included analytical sample replication and certified reference material (DOLT-4, National Research Council of Canada). The mean relative percent difference (standard deviation [SD] /mean) for analytical sample replication was 10.0% for MeHg, 9.5% for Hg(II), and 7.1% for THg. The mean recoveries for the certified reference material (n = 4) was 99.9% for MeHg, 107.9% for Hg(II), and 103.7% for THg. Analytical detection limits (3 ⁄ SD of reagent blanks) were 0.29 pg for MeHg and 2.41 pg for Hg(II). Method detection limits (4 ⁄ SD of method blanks) were 1.31 pg for MeHg and 23.01 pg for Hg(II). All samples were well above detection limits. Kolmogorov–Smirnov tests indicated that data distributions for some species did not approximate normality, so we used conservative, non-parametric Kruskal–Wallis (KW) tests to assess whether there were overall significant differences (p < 0.05) in MeHg and THg concentrations among species. We followed this with Dunn’s Multiple Comparison test if the KW test was significant, to determine which species had MeHg or THg values significantly different from each other. All tests were conducted with InStat (GraphPad Software, 2009). There was considerable interspecific variation in Hg concentrations derived from primary feathers, which led to significant differences in median values among the six species for both THg (KW = 31.1, n = 44, p < 0.001) and MeHg (KW = 27.0, n = 44, p < 0.001). For both types of Hg, highest concentrations were found in ivory gull and lowest were in common eider (Table 1). Ivory gull also had the largest range in values and the highest coefficient of variation for both THg and MeHg. Comparing THg and MeHg medians among species, ivory gull had significantly higher Hg values than common eider (Dunn’s Multiple Comparisons Test, p < 0.001) and thick-billed murre (p < 0.05), while northern fulmar had higher Hg feather concentrations than common eider (p < 0.01). In fact, the minimum THg in all three types of ivory gull feathers was higher than the maximum THg in most other species. The highest measured THg was 43.66 lg/g dw in primary feathers from one ivory gull. Although body and tertial feathers of ivory gulls had lower median THg and MeHg than primary feathers (Table 1), these differences were not significant (KW = 1.1, n = 15, p > 0.6), presumably due to the small sample sizes and high variation among feather samples. There was also a significant difference in the proportion of MeHg/THg in primary feathers among sample species (KW = 28.3, n = 44, p < 0.001). The lowest MeHg/THg ratio was that of ivory gull (67%), which was 20% lower than the next lowest proportion in common eiders (Table 1). Our data on Hg in feathers of marine birds in the Canadian Arctic were consistent with previous studies on other avian tissues, and assuming that much of the Hg comes from local Arctic food supplies, these data suggest that contamination of Arctic marine birds by long-range transport of Hg emitted from locations in temperate and tropical regions continues to be a serious environmental concern (Braune et al., 2006, 2010). Based on available tracking data or information on arrival and nesting dates, the six species in our pilot study use Arctic food webs as their main source of nutrients to form their eggs or to grow the feathers we analyzed (Gaston and Hipfner, 2000; Goudie et al., 2000; Mosbech et al., 2006; Mallory et al., 2008c; Frederiksen et al., 2012; Sénéchal et al., 2011; Spencer et al., 2014). We found that MeHg concentrations in feathers of Canadian Arctic marine birds (Table 1) spanned much of the range reported in studies from tropical to polar regions (from various feather types; means of 0.43–28.0 lg/g dw;
Please cite this article in press as: Mallory, M.L., et al. Mercury concentrations in feathers of marine birds in Arctic Canada. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.043
M.L. Mallory et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
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Fig. 1. Map of sampling sites of marine bird populations in the Canadian Arctic. Feathers from marine bird species were collected as follows: ivory gulls were sampled at Seymour Island (1), glaucous gulls were sampled at Nasaruvaalik Island (2); thick-billed murres, northern fulmars, and black-legged kittiwakes were sampled at Prince Leopold Island (3); common eiders were sampled near Cape Dorset (4).
Thompson et al., 1992a,b, 1993, 1998; Burger and Gochfeld, 2000; Burger, 2002; Burger et al., 2008), although average values were lower than the extremes measured in Tristan albatross (Diomedea dabbenena, 28.0 ± 14.3; Thompson et al., 1993) and wandering albatross (Diomedea exulans, 20.1 ± 7.6; Tavares et al., 2013). Furthermore, Hg generally varied predictably across the established trophic positions of these species (based on earlier studies in this region; Akearok et al., 2010; Mallory and Braune,
2012; Provencher et al., 2014), suggesting that feathers were useful proxies of Hg concentrations in the Arctic environment. Perhaps the most important result in our study was the observation that feather Hg concentration in the ivory gull was exceptionally high and variable among nesting birds, similar to the pattern observed in their eggs (Braune et al., 2006; Akearok et al., 2010) and that of other Arctic birds feeding at high trophic levels (Atwell et al., 1998). In fact, the value of 43.66 lg/g dw
Please cite this article in press as: Mallory, M.L., et al. Mercury concentrations in feathers of marine birds in Arctic Canada. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.043
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Table 1 Descriptive statistics of THg and MeHg analysis (concentrations in lg/g dw) in primary feathers of Arctic marine birds. Species are ivory gull (IVGU), glaucous gull (GLGU), blacklegged kittiwake (BLKI), common eider (COEI), thick-billed murre (TBMU) and northern fulmar (NOFU); IVGUp represents primary feathers, IVGUb represent body feathers, IVGUt represents tertial feathers. %MeHg is the proportion of MeHg:THg in feathers as a percentage. Species
IVGUp IVGUb IVGUt GLGU BLKI COEI TBMU NOFU a b
n
8 4 3 4 2 10 10 10
Feather THg
Feather MeHg
Mean (SD) feather %MeHg
Mean (SD), median, range
CV (%)
Mean (SD), median, range
CV (%)
15.79 (14.13), 13.70, 4.31–43.66 11.66 (6.52), 10.37, 5.30–20.62 6.20 (1.28), 6.64, 4.76–7.19 2.31 (1.68), 1.82, 0.62–6.82 3.58 (0.92), 3.58, 2.66–4.50 0.59 (0.21), 0.59, 0.24–0.95 1.94 (0.63), 1.82, 1.19–3.04 2.71 (0.72), 2.39, 1.86–3.97
89 56 21 73 26 36 32 27
11.28 (9.92), 9.74, 0.50–27.88 9.42 (5.31), 8.12, 4.60–16.85 4.62 (0.99), 4.61, 3.64–5.62 2.14 (1.66), 1.64, 0.58–6.62 3.27 (0.87), 3.27, 2.40–4.14 0.52 (0.19), 0.52, 0.21–0.84 1.73 (0.58), 1.65, 1.05–2.72 2.37 (0.65), 2.10, 1.56–3.54
88 56 21 77 26 37 33 27
Egg THga
THgfeather:THgegg
Mean (SD), n 67 81 75 91 91 87 90 88
(16) (4) (5) (4) (2) (1) (1)
6.37 (5.17), 6.37 (5.17), 6.37 (5.17), 0.44, 2b 0.82 (0.09), 0.35 (0.02), 1.33 (0.28), 1.41 (0.11),
6 6 6 12 18 15 15
2.5 1.8 1.0 5.2 4.4 1.7 1.5 1.9
From Akearok et al. (2010). M.L. Mallory, unpubl. data from this field location.
observed in some ivory gull primary feathers was among the highest reported in wild birds, and near the maxima reported in wandering albatross body feathers (57.2 lg/g; Tavares et al., 2013). Bond et al. (2015) found a 45-fold increase in ivory gull body feather MeHg between 1877 and 2007, with a maximum measured MeHg in feathers of 11.51 lg/g from an ivory gull collected in 1952, and a modeled feather MeHg value for 2007 of 4.11 lg/g. From samples collected in the field in 2010, our mean and maximum measured MeHg in ivory gull body feathers were 1.5–2.3 higher than what Bond et al. (2015) reported, suggesting that Hg has continued to increase in these birds. Therefore, our study reasserts the contention of Braune et al. (2006) and Bond et al. (2015) that Hg concentrations in ivory gulls may be sufficiently elevated to have sublethal effects on the species. A key element in the concern for the ivory gull is that this species remains year-round in locations well removed from any sources of emissions or pollution (Spencer et al., 2014), and thus it accumulates these very high concentrations of Hg through long-range transport and biomagnification in Arctic food webs. We also found an interesting pattern in the ratio of THg in feathers to that in eggs among the six species. The ratio of THgfeather:THgegg was over twice as high in glaucous gull and black-legged kittiwake compared to ivory gull, thick-billed murre, northern fulmar and common eider (Table 1). This was not simply attributable to glaucous gull and black-legged kittiwake females laying larger clutches, thereby reducing the relative amount of mercury in any single egg, since common eider and ivory gull females also lay multi-egg clutches (northern fulmar and thick-billed murre females lay a single egg). Given our small sample sizes, the fact that we did not take eggs and feathers from the same individuals, and that we did not control for age or sex (all factors that can markedly influence Hg concentrations in feathers; Braune, 1987; Braune and Gaskin, 1987; Robinson et al., 2012), our observations are speculative at this time. Clearly more data are required to determine if this pattern among species is an accurate reflection of relative Hg in these two tissues. We note, however, that despite this uncertainty, our black-legged kittiwake THgfeather values (3.58 lg/g dw; n = 2) were in the same range as reported elsewhere (2.91–5.5 lg/g dw; Thompson et al., 1992a; Burger et al., 2008), and the mean THgegg (0.82 lg/g dw; Akearok et al., 2010) is consistent with long term patterns (Braune, 2007). Moreover, previous research has suggested that contaminants in these two species are somewhat anomalous compared to the other four marine bird species. For example, Braune et al. (2002) showed that levels of contaminants in the glaucous gull vary markedly across the Arctic, presumably influenced by their broad, opportunistic diet, and the observation of high individual specialization in feeding (Bustnes et al., 2000; Weiser and Gilchrist, 2012). As well, Akearok et al. (2010: Figure 2) found that the black-legged
kittiwake had the third lowest concentration of THgegg among nine Arctic-breeding bird species, including all of those in this study, and black-legged kittiwake THgegg concentrations were much lower than would be predicted for its trophic position (Provencher et al., 2014). Because other gulls in the Canadian Arctic are income breeders, gathering nutrients for egg production from the environment near their colony (Hobson et al., 2000), we assumed that the glaucous gull and black-legged kittiwake do the same (in agreement with tracking data), and thus should be accruing relatively high concentrations of Hg. In Svalbard, black-legged kittiwake Hg concentrations decline from early in the breeding season through to the autumn (Øverjordet et al., 2015), presumably due to shifting diets. We suggest three possible explanations why glaucous gull and black-legged kittiwake appear to have much higher Hg in feathers than their eggs, which merit future study. First, these two species might exhibit major shifts in diet between wintering/migration areas, breeding and molting periods, which cause birds to arrive in the Arctic with relatively low body Hg concentrations but accrue higher Hg that is depurated to feathers during molt (but this would be counter to results on glaucous-winged gulls Larus glaucescens, Hobson and Bond, 2012). Second, these species may be able to demethylate and process Hg differently than the other species (Bond and Diamond, 2009). Third, despite field observations and patterns from other gulls, black-legged kittiwake and glaucous gull may use proportionally more endogenous reserves for egg production, and these reserves are stored from diets much lower in Hg. Interestingly, Braune (2007) showed that THgegg increased from 1976 to 2003 for northern fulmar and thick-billed murre at Prince Leopold Island in the Canadian high Arctic, but there was no significant trend for black-legged kittiwake at the same colony over the same time period. The principal form of mercury in feathers is MeHg, typically comprising >90% in most species (e.g., Bond and Diamond, 2009). However, we found that MeHg averaged 67–81% of the THg in ivory gull feathers, unexpectedly lower than other species. We posit two possible explanations for this difference. First, ivory gulls may have a higher capacity to demethylate Hg than other species, as their trophic position and diet suggests that they have higher year-round exposure (e.g., Braune et al., 2006). There is evidence that across species, the proportion of THg appearing as MeHg decreases with increasing THg (e.g., Thompson et al., 1990; Bond and Diamond, 2009). Second, UV radiation plays a large role in demethylation of environmental mercury in freshwater lakes (Lehnherr and St. Louis, 2009), and we speculate that it may have an effect on MeHg photodemethylation in semi-opaque tissues as well, like the translucent feathers of the ivory gull. Bond et al. (2015) found relatively lower percent MeHg in recent ivory gull feathers. The few articles discussing this topic suggest that MeHg
Please cite this article in press as: Mallory, M.L., et al. Mercury concentrations in feathers of marine birds in Arctic Canada. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.043
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forms stable sulfur based complexes with keratin in feathers, but studies show that UV exposure may break down keratin or other compounds in feathers (e.g., Blanco et al., 2005). Because ivory gull feathers are almost translucent, it is conceivable that radiation penetrates the feathers to a greater amount than the more opaque feathers of other species, causing photoreactions or increased keratin breakdown, which could release mercury species and result in the photodegradation of MeHg species. This hypothesis merits further study, however, as other pale-feathered Arctic species (gulls, terns) exposed to similar, high levels of sunlight do not show this pattern (Bond and Diamond, 2009; this study). Our pilot project established feather Hg reference values for six species of marine birds breeding in the Canadian Arctic, and considering the recent findings of Bond et al. (2015), we have provided additional, strong evidence that Hg may be an issue of particular concern for ivory gulls. A logical next step in this research is to assess the spatiotemporal pattern of feather Hg in these species, including museum specimen as in other studies (e.g., Thompson et al., 1992b; Bond et al., 2015). This would allow researchers to examine regional variation in Hg, whether feather Hg patterns from the past century (e.g., Thompson et al., 1992b; Bond et al., 2015) confirm more recent patterns established from monitoring of eggs (Braune, 2007), and perhaps invoking stable isotopes of carbon, nitrogen and mercury (Blum et al., 2014) to assess if Hg sources have changed through time in Arctic food webs. Acknowledgements We thank the many field assistants who helped collect these samples, Mia Pelletier for send the glaucous gull feathers, and Tony Gaston and Alex Bond for reviewing the manuscript. Financial and logistic support were provided by Environment Canada (Canadian Wildlife Service, Wildlife Research Division), Natural Resources Canada (Polar Continental Shelf Program), Natural Sciences and Engineering Research Council, the Canada Research Chairs Program, and Aboriginal Affairs and Northern Development Canada (International Polar Year, Northern Contaminants Program). All collections were made with appropriate federal and territorial permits. References Ackerman, J.T., Herzog, M.P., Schwarzbach, S.E., 2013. Methylmercury is the predominant form of mercury in bird eggs: a synthesis. Environ. Sci. Technol. 47, 2052–2060. Akearok, J., Hebert, C., Braune, B.M., Mallory, M.L., 2010. Inter- and intraclutch variation in egg mercury levels in marine birds species from the Canadian high Arctic. Sci. Total Environ. 408, 836–840. Appelquist, H., Asbirk, S., Drabæk, I., 1984. Mercury monitoring: mercury stability in bird feathers. Mar. Pollut. Bull. 15, 22–24. Atwell, L., Hobson, K.A., Welch, H.E., 1998. Biomagnification and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen isotope analysis. Can. J. Fish. Aquat. Sci. 55, 1114–1121. Blanco, G., Frias, O., Garrido-Frenandez, J., Hornero-Mendez, D., 2005. Environmental-induced acquisition of nuptial plumage expression: a role of denaturation of feather carotenoproteins? Proc. R. Soc. B 272, 1893–1900. Blum, J.D., Sherman, L.S., Johnson, M.W., 2014. Mercury isotopes in earth and environmental sciences. Ann. Rev. Earth Planet Sci. 42, 249–269. Bond, A.L., Diamond, A.W., 2009. Total and methyl mercury concentrations in seabird feathers and eggs. Arch. Environ. Contam. Toxicol. 56, 286–291. Bond, A.L., Hobson, K.A., Branfireun, B.A., 2015. Rapidly increasing methylmercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record. Proc. R. Soc. B 282, 2015032. http://dx.doi.org/10.1098/rspb.2015.0032. Braune, B.M., 1987. Comparison of total mercury levels in relation to diet and molt for nine species of marine birds. Arch. Environ. Contam. Toxicol. 16, 217–224. Braune, B.M., 2007. Temporal trends of organochlorines and mercury in seabird eggs from the Canadian Arctic, 1975–2003. Environ. Pollut. 148, 599–613. Braune, B.M., Gaskin, D.E., 1987. A mercury budget for the Bonaparte’s gull during autumn moult. Ornis Scand. 18, 244–250. Braune, B.M., Donaldson, G.M., Hobson, K.A., 2002. Contaminant residues in seabird eggs from the Canadian Arctic. II. Spatial trends and evidence from stable isotopes for intercolony differences. Environ. Pollut. 117, 133–145.
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Baseline
Mercury concentrations in feathers of marine birds in Arctic Canada Mark L. Mallory a,⇑, Birgit M. Braune b, Jennifer F. Provencher c, D. Benjamin Callaghan a, H. Grant Gilchrist b, Samuel T. Edmonds d,1, Karel Allard e, Nelson J. O’Driscoll d a
Department of Biology, Acadia University, 15 University Drive, Wolfville, Nova Scotia B4P 2R6, Canada National Wildlife Research Centre, Environment Canada, Raven Road, Carleton University, Ottawa, Ontario K1A 0H3, Canada c Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1A 0H3, Canada d Department of Earth and Environmental Science, Acadia University, 15 University Drive, Wolfville, Nova Scotia B4P 2R6, Canada e Environment Canada, 17 Waterfowl Lane, Sackville, New Brunswick E4L 1G6, Canada b
a r t i c l e
i n f o
Article history: Received 27 April 2015 Revised 22 June 2015 Accepted 25 June 2015 Available online xxxx Keywords: Arctic Marine bird Mercury Ivory gull Photodemethylation
a b s t r a c t Mercury (Hg) concentrations are a concern in the Canadian Arctic, because they are relatively high compared to background levels and to similar species farther south, and are increasing in many wildlife species. Among marine birds breeding in the Canadian Arctic, Hg concentrations have been monitored regularly in eggs and intermittently in livers, but feathers have generally not been used as an indicator of Hg exposure or burden. We examined Hg concentrations in six marine bird species in the Canadian Arctic. Ivory gull Pagophila eburnea, feather Hg was exceptionally high, while glaucous gull Larus hyperboreus feather Hg was unexpectedly low, and ratios of feather THg to egg THg varied across species. The proportion of total Hg that was comprised of methyl Hg in ivory gull feathers was lower than in other species, and may be related to photo-demethylation or keratin breakdown in semi-opaque feather tissue. Ó 2015 Elsevier Ltd. All rights reserved.
Mercury (Hg) concentrations are elevated in many ecosystems across the Canadian Arctic (Dietz et al., 2013; Lavoie et al., 2013). Different forms of mercury (species) occur in the environment, with methylmercury (MeHg) readily accumulating in organisms due to its affinity for cellular proteins (Dietz et al., 2013), and thereby accounting for the majority of the mercury found within tissues in higher trophic levels of a system (>90%; Ackerman et al., 2013), compared to inorganic mercury species. MeHg may be detrimental to organisms because it has negative impacts on their physiology, including acting as a neurotoxin and immunotoxin (Wolfe et al., 1998). Methylmercury will biomagnify in food webs by a factor of 4–10 per trophic step (Kidd et al., 2011; Lavoie et al., 2013). Hence, organisms feeding at high trophic levels may accrue high concentrations of MeHg. This is particularly evident in Arctic marine birds (Braune et al., 2002, 2006, 2014). To date, most Hg research on marine birds in the Canadian Arctic has examined concentrations in liver, muscle or egg tissues (Mallory and Braune, 2012). However, for most seabirds in the Canadian Arctic, sampling Hg in feathers has not been undertaken to date, despite the advantages that the bird or egg does not need to be destroyed during sampling (a particular benefit in the case of
⇑ Corresponding author. 1
E-mail address: [email protected] (M.L. Mallory). Current address: TRC, Inc, 14 Gabriel Dr, Augusta, ME 04330, USA.
rare species), shed feathers may be taken from nests, and that feathers are chemically stable (i.e., Hg concentrations do not change in feathers once they are grown; Appelquist et al., 1984). Concentrations of Hg in feathers can vary markedly depending on sex, age and molt sequence (Braune and Gaskin, 1987; Bond and Diamond, 2009), and therefore knowledge of species molt patterns and chronology is essential for interpreting Hg concentrations from feathers. Despite variation among feathers and feather groups, feather sampling has enabled determination of Hg load in certain marine bird species (reviewed in Burger, 1993), including for example northern fulmar Fulmarus glacialis (Thompson et al., 1992a,b), Bonaparte’s gull Larus philadelphia (Braune and Gaskin, 1987), herring gull Larus argentatus (Thompson et al., 1993), and albatrosses (Tavares et al., 2013). Recently, Bond et al. (2015) found a disconcerting pattern in MeHg in feathers from one Arctic seabird, the ivory gull (Pagophila eburnea), an endangered species in Canada. Using breast feathers from museum specimens, they measured a 45-fold increase in MeHg in ivory gull feathers over the period 1877– 2007, and argued that Hg loads may have contributed to the decline of this species in the past three decades (Gilchrist and Mallory, 2005). We conducted a pilot study to assess Hg variation in primary feathers across marine bird species breeding in Arctic Canada, to establish reference values for these birds, and in particular for
http://dx.doi.org/10.1016/j.marpolbul.2015.06.043 0025-326X/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Mallory, M.L., et al. Mercury concentrations in feathers of marine birds in Arctic Canada. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.043
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two of the key gull species identified by Provencher et al. (2014) for concern with Hg levels, ivory gull and glaucous gull (Larus hyperboreus). If concentrations of Hg in feathers varied according to the known trophic position of each species (as they vary in eggs and livers; Provencher et al., 2014), then we predicted that: (1) across bird species, total mercury (THg) and methylmercury (MeHg) concentrations in feathers would be higher in birds occupying higher trophic positions; and (2) mercury concentrations found in feathers would be correlated with those in the literature for mercury concentrations in eggs. Feather samples of six species of Canadian Arctic-breeding marine birds were collected from 2009 to 2011 from four locations in the Canadian Arctic (Nunavut Territory; Fig. 1), the same locations where eggs have been monitored for Hg (Braune et al., 2006; Akearok et al., 2010). While the ivory gull remains in Arctic waters year-round (Spencer et al., 2014), the other bird species likely spend the winter south of the Arctic in coastal and offshore waters of the northwest Atlantic Ocean (Mosbech et al., 2006; Mallory et al., 2008a; Gaston et al., 2011; Frederiksen et al., 2012). We wanted to compare Hg concentrations in feathers that had been grown by marine birds while in the Arctic, and presumably when relying on foods acquired in the Arctic to supply much of the nutrients for feather growth (although some Hg would reflect longer-term concentrations in the body from year-round exposure). Consequently, we referred to published guides reporting the known feather molt patterns of these species (Ginn and Melville, 1983; Gaston and Hipfner, 2000; Goudie et al., 2000; Mallory et al., 2008b, 2012a,b; Weiser and Gilchrist, 2012) to select feathers grown while the birds were in the Arctic. For all species, this meant analyzing one of their inner primary (flight) feathers, which would have been among those grown during or shortly after the previous breeding season prior to southward migration. However, for the ivory gull, a species that spends its entire year in Arctic waters, we also analyzed some body and tertial feathers, as the collection of feathers from nests was opportunistic. Because Hg content can vary with feather position and molt sequence (Braune, 1987; Head et al., 2011), we standardized to the extent possible by sampling the same feathers within and across species. Primary feathers (position 1, 2 or 3) were collected for analysis from carcasses of thick-billed murre (Uria lomvia; n = 10), northern fulmar (n = 10), and black-legged kittiwake (Rissa tridactyla; n = 2) at Prince Leopold Island (74°N, 90°W) in 2009 as part of an International Polar Year project (Gaston et al., 2011). Shed feathers of ivory gull (P. eburnea; n = 8) were collected in 2010 from eight different nests on Seymour Island (Mallory et al., 2012a); these were mostly primary feathers (estimated positions 2–5), although some body feathers and tertials were collected. Primary feathers (position 2, 3 of three birds, position 4, 5 of one bird) of glaucous gull (L. hyperboreus; n = 4) were sampled in 2010 from carcasses collected from Nasaruvaalik Island (75.8°N, 96.3°W) as part of a long-term study at that site (Mallory et al., 2012b). Primary feathers (position 1, 2 or 3) of common eider (Somateria mollissima borealis; n = 10) were collected in 2011 from carcasses of birds sampled near Cape Dorset (64.2°N, 76.6°W; Provencher, 2013). We analyzed THg from the third primary and MeHg from the second primary, with the exception of the one glaucous gull (above) and ivory gull feathers. Sample feathers were cleaned for analysis by washing three times with Milli-Q water and were then oven-dried overnight at 60 °C. The weight of the dry feathers was measured to the nearest 0.1 mg and recorded. Those feathers weighing 650 mg were digested in 10 mL of 25% KOH/MeOH solution, while those >50 mg were digested in 40 mL of 25% KOH/MeOH solution. A sample aliquot (20 lL) of the digested sample was transferred to a reaction bubbler and analyzed for MeHg and inorganic Hg content through ethylation with NaB(C2H5)4 and purge-and-trap gas
chromatography prior to detection by atomic fluorescence spectroscopy (Brooks Rand Model III) by Florida Department of Environmental Protection method HG-003-2.10 (Edmonds et al., 2012). Concurrent calibration for MeHg and Hg(II) was performed and THg was determined by addition of inorganic and methylmercury values. Internal quality control included analytical sample replication and certified reference material (DOLT-4, National Research Council of Canada). The mean relative percent difference (standard deviation [SD] /mean) for analytical sample replication was 10.0% for MeHg, 9.5% for Hg(II), and 7.1% for THg. The mean recoveries for the certified reference material (n = 4) was 99.9% for MeHg, 107.9% for Hg(II), and 103.7% for THg. Analytical detection limits (3 ⁄ SD of reagent blanks) were 0.29 pg for MeHg and 2.41 pg for Hg(II). Method detection limits (4 ⁄ SD of method blanks) were 1.31 pg for MeHg and 23.01 pg for Hg(II). All samples were well above detection limits. Kolmogorov–Smirnov tests indicated that data distributions for some species did not approximate normality, so we used conservative, non-parametric Kruskal–Wallis (KW) tests to assess whether there were overall significant differences (p < 0.05) in MeHg and THg concentrations among species. We followed this with Dunn’s Multiple Comparison test if the KW test was significant, to determine which species had MeHg or THg values significantly different from each other. All tests were conducted with InStat (GraphPad Software, 2009). There was considerable interspecific variation in Hg concentrations derived from primary feathers, which led to significant differences in median values among the six species for both THg (KW = 31.1, n = 44, p < 0.001) and MeHg (KW = 27.0, n = 44, p < 0.001). For both types of Hg, highest concentrations were found in ivory gull and lowest were in common eider (Table 1). Ivory gull also had the largest range in values and the highest coefficient of variation for both THg and MeHg. Comparing THg and MeHg medians among species, ivory gull had significantly higher Hg values than common eider (Dunn’s Multiple Comparisons Test, p < 0.001) and thick-billed murre (p < 0.05), while northern fulmar had higher Hg feather concentrations than common eider (p < 0.01). In fact, the minimum THg in all three types of ivory gull feathers was higher than the maximum THg in most other species. The highest measured THg was 43.66 lg/g dw in primary feathers from one ivory gull. Although body and tertial feathers of ivory gulls had lower median THg and MeHg than primary feathers (Table 1), these differences were not significant (KW = 1.1, n = 15, p > 0.6), presumably due to the small sample sizes and high variation among feather samples. There was also a significant difference in the proportion of MeHg/THg in primary feathers among sample species (KW = 28.3, n = 44, p < 0.001). The lowest MeHg/THg ratio was that of ivory gull (67%), which was 20% lower than the next lowest proportion in common eiders (Table 1). Our data on Hg in feathers of marine birds in the Canadian Arctic were consistent with previous studies on other avian tissues, and assuming that much of the Hg comes from local Arctic food supplies, these data suggest that contamination of Arctic marine birds by long-range transport of Hg emitted from locations in temperate and tropical regions continues to be a serious environmental concern (Braune et al., 2006, 2010). Based on available tracking data or information on arrival and nesting dates, the six species in our pilot study use Arctic food webs as their main source of nutrients to form their eggs or to grow the feathers we analyzed (Gaston and Hipfner, 2000; Goudie et al., 2000; Mosbech et al., 2006; Mallory et al., 2008c; Frederiksen et al., 2012; Sénéchal et al., 2011; Spencer et al., 2014). We found that MeHg concentrations in feathers of Canadian Arctic marine birds (Table 1) spanned much of the range reported in studies from tropical to polar regions (from various feather types; means of 0.43–28.0 lg/g dw;
Please cite this article in press as: Mallory, M.L., et al. Mercury concentrations in feathers of marine birds in Arctic Canada. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.043
M.L. Mallory et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
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Fig. 1. Map of sampling sites of marine bird populations in the Canadian Arctic. Feathers from marine bird species were collected as follows: ivory gulls were sampled at Seymour Island (1), glaucous gulls were sampled at Nasaruvaalik Island (2); thick-billed murres, northern fulmars, and black-legged kittiwakes were sampled at Prince Leopold Island (3); common eiders were sampled near Cape Dorset (4).
Thompson et al., 1992a,b, 1993, 1998; Burger and Gochfeld, 2000; Burger, 2002; Burger et al., 2008), although average values were lower than the extremes measured in Tristan albatross (Diomedea dabbenena, 28.0 ± 14.3; Thompson et al., 1993) and wandering albatross (Diomedea exulans, 20.1 ± 7.6; Tavares et al., 2013). Furthermore, Hg generally varied predictably across the established trophic positions of these species (based on earlier studies in this region; Akearok et al., 2010; Mallory and Braune,
2012; Provencher et al., 2014), suggesting that feathers were useful proxies of Hg concentrations in the Arctic environment. Perhaps the most important result in our study was the observation that feather Hg concentration in the ivory gull was exceptionally high and variable among nesting birds, similar to the pattern observed in their eggs (Braune et al., 2006; Akearok et al., 2010) and that of other Arctic birds feeding at high trophic levels (Atwell et al., 1998). In fact, the value of 43.66 lg/g dw
Please cite this article in press as: Mallory, M.L., et al. Mercury concentrations in feathers of marine birds in Arctic Canada. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.043
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Table 1 Descriptive statistics of THg and MeHg analysis (concentrations in lg/g dw) in primary feathers of Arctic marine birds. Species are ivory gull (IVGU), glaucous gull (GLGU), blacklegged kittiwake (BLKI), common eider (COEI), thick-billed murre (TBMU) and northern fulmar (NOFU); IVGUp represents primary feathers, IVGUb represent body feathers, IVGUt represents tertial feathers. %MeHg is the proportion of MeHg:THg in feathers as a percentage. Species
IVGUp IVGUb IVGUt GLGU BLKI COEI TBMU NOFU a b
n
8 4 3 4 2 10 10 10
Feather THg
Feather MeHg
Mean (SD) feather %MeHg
Mean (SD), median, range
CV (%)
Mean (SD), median, range
CV (%)
15.79 (14.13), 13.70, 4.31–43.66 11.66 (6.52), 10.37, 5.30–20.62 6.20 (1.28), 6.64, 4.76–7.19 2.31 (1.68), 1.82, 0.62–6.82 3.58 (0.92), 3.58, 2.66–4.50 0.59 (0.21), 0.59, 0.24–0.95 1.94 (0.63), 1.82, 1.19–3.04 2.71 (0.72), 2.39, 1.86–3.97
89 56 21 73 26 36 32 27
11.28 (9.92), 9.74, 0.50–27.88 9.42 (5.31), 8.12, 4.60–16.85 4.62 (0.99), 4.61, 3.64–5.62 2.14 (1.66), 1.64, 0.58–6.62 3.27 (0.87), 3.27, 2.40–4.14 0.52 (0.19), 0.52, 0.21–0.84 1.73 (0.58), 1.65, 1.05–2.72 2.37 (0.65), 2.10, 1.56–3.54
88 56 21 77 26 37 33 27
Egg THga
THgfeather:THgegg
Mean (SD), n 67 81 75 91 91 87 90 88
(16) (4) (5) (4) (2) (1) (1)
6.37 (5.17), 6.37 (5.17), 6.37 (5.17), 0.44, 2b 0.82 (0.09), 0.35 (0.02), 1.33 (0.28), 1.41 (0.11),
6 6 6 12 18 15 15
2.5 1.8 1.0 5.2 4.4 1.7 1.5 1.9
From Akearok et al. (2010). M.L. Mallory, unpubl. data from this field location.
observed in some ivory gull primary feathers was among the highest reported in wild birds, and near the maxima reported in wandering albatross body feathers (57.2 lg/g; Tavares et al., 2013). Bond et al. (2015) found a 45-fold increase in ivory gull body feather MeHg between 1877 and 2007, with a maximum measured MeHg in feathers of 11.51 lg/g from an ivory gull collected in 1952, and a modeled feather MeHg value for 2007 of 4.11 lg/g. From samples collected in the field in 2010, our mean and maximum measured MeHg in ivory gull body feathers were 1.5–2.3 higher than what Bond et al. (2015) reported, suggesting that Hg has continued to increase in these birds. Therefore, our study reasserts the contention of Braune et al. (2006) and Bond et al. (2015) that Hg concentrations in ivory gulls may be sufficiently elevated to have sublethal effects on the species. A key element in the concern for the ivory gull is that this species remains year-round in locations well removed from any sources of emissions or pollution (Spencer et al., 2014), and thus it accumulates these very high concentrations of Hg through long-range transport and biomagnification in Arctic food webs. We also found an interesting pattern in the ratio of THg in feathers to that in eggs among the six species. The ratio of THgfeather:THgegg was over twice as high in glaucous gull and black-legged kittiwake compared to ivory gull, thick-billed murre, northern fulmar and common eider (Table 1). This was not simply attributable to glaucous gull and black-legged kittiwake females laying larger clutches, thereby reducing the relative amount of mercury in any single egg, since common eider and ivory gull females also lay multi-egg clutches (northern fulmar and thick-billed murre females lay a single egg). Given our small sample sizes, the fact that we did not take eggs and feathers from the same individuals, and that we did not control for age or sex (all factors that can markedly influence Hg concentrations in feathers; Braune, 1987; Braune and Gaskin, 1987; Robinson et al., 2012), our observations are speculative at this time. Clearly more data are required to determine if this pattern among species is an accurate reflection of relative Hg in these two tissues. We note, however, that despite this uncertainty, our black-legged kittiwake THgfeather values (3.58 lg/g dw; n = 2) were in the same range as reported elsewhere (2.91–5.5 lg/g dw; Thompson et al., 1992a; Burger et al., 2008), and the mean THgegg (0.82 lg/g dw; Akearok et al., 2010) is consistent with long term patterns (Braune, 2007). Moreover, previous research has suggested that contaminants in these two species are somewhat anomalous compared to the other four marine bird species. For example, Braune et al. (2002) showed that levels of contaminants in the glaucous gull vary markedly across the Arctic, presumably influenced by their broad, opportunistic diet, and the observation of high individual specialization in feeding (Bustnes et al., 2000; Weiser and Gilchrist, 2012). As well, Akearok et al. (2010: Figure 2) found that the black-legged
kittiwake had the third lowest concentration of THgegg among nine Arctic-breeding bird species, including all of those in this study, and black-legged kittiwake THgegg concentrations were much lower than would be predicted for its trophic position (Provencher et al., 2014). Because other gulls in the Canadian Arctic are income breeders, gathering nutrients for egg production from the environment near their colony (Hobson et al., 2000), we assumed that the glaucous gull and black-legged kittiwake do the same (in agreement with tracking data), and thus should be accruing relatively high concentrations of Hg. In Svalbard, black-legged kittiwake Hg concentrations decline from early in the breeding season through to the autumn (Øverjordet et al., 2015), presumably due to shifting diets. We suggest three possible explanations why glaucous gull and black-legged kittiwake appear to have much higher Hg in feathers than their eggs, which merit future study. First, these two species might exhibit major shifts in diet between wintering/migration areas, breeding and molting periods, which cause birds to arrive in the Arctic with relatively low body Hg concentrations but accrue higher Hg that is depurated to feathers during molt (but this would be counter to results on glaucous-winged gulls Larus glaucescens, Hobson and Bond, 2012). Second, these species may be able to demethylate and process Hg differently than the other species (Bond and Diamond, 2009). Third, despite field observations and patterns from other gulls, black-legged kittiwake and glaucous gull may use proportionally more endogenous reserves for egg production, and these reserves are stored from diets much lower in Hg. Interestingly, Braune (2007) showed that THgegg increased from 1976 to 2003 for northern fulmar and thick-billed murre at Prince Leopold Island in the Canadian high Arctic, but there was no significant trend for black-legged kittiwake at the same colony over the same time period. The principal form of mercury in feathers is MeHg, typically comprising >90% in most species (e.g., Bond and Diamond, 2009). However, we found that MeHg averaged 67–81% of the THg in ivory gull feathers, unexpectedly lower than other species. We posit two possible explanations for this difference. First, ivory gulls may have a higher capacity to demethylate Hg than other species, as their trophic position and diet suggests that they have higher year-round exposure (e.g., Braune et al., 2006). There is evidence that across species, the proportion of THg appearing as MeHg decreases with increasing THg (e.g., Thompson et al., 1990; Bond and Diamond, 2009). Second, UV radiation plays a large role in demethylation of environmental mercury in freshwater lakes (Lehnherr and St. Louis, 2009), and we speculate that it may have an effect on MeHg photodemethylation in semi-opaque tissues as well, like the translucent feathers of the ivory gull. Bond et al. (2015) found relatively lower percent MeHg in recent ivory gull feathers. The few articles discussing this topic suggest that MeHg
Please cite this article in press as: Mallory, M.L., et al. Mercury concentrations in feathers of marine birds in Arctic Canada. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.043
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forms stable sulfur based complexes with keratin in feathers, but studies show that UV exposure may break down keratin or other compounds in feathers (e.g., Blanco et al., 2005). Because ivory gull feathers are almost translucent, it is conceivable that radiation penetrates the feathers to a greater amount than the more opaque feathers of other species, causing photoreactions or increased keratin breakdown, which could release mercury species and result in the photodegradation of MeHg species. This hypothesis merits further study, however, as other pale-feathered Arctic species (gulls, terns) exposed to similar, high levels of sunlight do not show this pattern (Bond and Diamond, 2009; this study). Our pilot project established feather Hg reference values for six species of marine birds breeding in the Canadian Arctic, and considering the recent findings of Bond et al. (2015), we have provided additional, strong evidence that Hg may be an issue of particular concern for ivory gulls. A logical next step in this research is to assess the spatiotemporal pattern of feather Hg in these species, including museum specimen as in other studies (e.g., Thompson et al., 1992b; Bond et al., 2015). This would allow researchers to examine regional variation in Hg, whether feather Hg patterns from the past century (e.g., Thompson et al., 1992b; Bond et al., 2015) confirm more recent patterns established from monitoring of eggs (Braune, 2007), and perhaps invoking stable isotopes of carbon, nitrogen and mercury (Blum et al., 2014) to assess if Hg sources have changed through time in Arctic food webs. Acknowledgements We thank the many field assistants who helped collect these samples, Mia Pelletier for send the glaucous gull feathers, and Tony Gaston and Alex Bond for reviewing the manuscript. Financial and logistic support were provided by Environment Canada (Canadian Wildlife Service, Wildlife Research Division), Natural Resources Canada (Polar Continental Shelf Program), Natural Sciences and Engineering Research Council, the Canada Research Chairs Program, and Aboriginal Affairs and Northern Development Canada (International Polar Year, Northern Contaminants Program). All collections were made with appropriate federal and territorial permits. References Ackerman, J.T., Herzog, M.P., Schwarzbach, S.E., 2013. Methylmercury is the predominant form of mercury in bird eggs: a synthesis. Environ. Sci. Technol. 47, 2052–2060. Akearok, J., Hebert, C., Braune, B.M., Mallory, M.L., 2010. Inter- and intraclutch variation in egg mercury levels in marine birds species from the Canadian high Arctic. Sci. Total Environ. 408, 836–840. Appelquist, H., Asbirk, S., Drabæk, I., 1984. Mercury monitoring: mercury stability in bird feathers. Mar. Pollut. Bull. 15, 22–24. Atwell, L., Hobson, K.A., Welch, H.E., 1998. Biomagnification and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen isotope analysis. Can. J. Fish. Aquat. Sci. 55, 1114–1121. Blanco, G., Frias, O., Garrido-Frenandez, J., Hornero-Mendez, D., 2005. Environmental-induced acquisition of nuptial plumage expression: a role of denaturation of feather carotenoproteins? Proc. R. Soc. B 272, 1893–1900. Blum, J.D., Sherman, L.S., Johnson, M.W., 2014. Mercury isotopes in earth and environmental sciences. Ann. Rev. Earth Planet Sci. 42, 249–269. Bond, A.L., Diamond, A.W., 2009. Total and methyl mercury concentrations in seabird feathers and eggs. Arch. Environ. Contam. Toxicol. 56, 286–291. Bond, A.L., Hobson, K.A., Branfireun, B.A., 2015. Rapidly increasing methylmercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record. Proc. R. Soc. B 282, 2015032. http://dx.doi.org/10.1098/rspb.2015.0032. Braune, B.M., 1987. Comparison of total mercury levels in relation to diet and molt for nine species of marine birds. Arch. Environ. Contam. Toxicol. 16, 217–224. Braune, B.M., 2007. Temporal trends of organochlorines and mercury in seabird eggs from the Canadian Arctic, 1975–2003. Environ. Pollut. 148, 599–613. Braune, B.M., Gaskin, D.E., 1987. A mercury budget for the Bonaparte’s gull during autumn moult. Ornis Scand. 18, 244–250. Braune, B.M., Donaldson, G.M., Hobson, K.A., 2002. Contaminant residues in seabird eggs from the Canadian Arctic. II. Spatial trends and evidence from stable isotopes for intercolony differences. Environ. Pollut. 117, 133–145.
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