Marine Pollution Bulletin xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
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: mark.mallory@acadiau.ca (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
2
M.L. Mallory et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
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
3
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
4
M.L. Mallory et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
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
M.L. Mallory et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
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.
5
Braune, B.M., Mallory, M.L., Gilchrist, H.G., 2006. Elevated mercury levels in a
declining population of Ivory Gulls in the Canadian Arctic. Mar. Pollut. Bull. 52,
978–982.
Braune, B.M., Mallory, M.L., Butt, C.M., Mabury, S., Muir, D., 2010. Persistent
halogenated organic contaminants and mercury in northern fulmars (Fulmarus
glacialis) from the Canadian Arctic. Environ. Pollut. 158, 3513–3519.
Braune, B.M., Gaston, A.J., Hobson, K.A., Gilchrist, H.G., Mallory, M.L., 2014. Changes
in food web structure alter trends of mercury uptake at two seabird colonies in
the Canadian Arctic. Environ. Sci. Technol. 48, 13246–13252.
Burger, J., 1993. Metals in avian feathers: bioindicators of environmental pollution.
Rev. Environ. Toxicol. 5, 203–311.
Burger, J., 2002. Food chain differences affect heavy metals in bird eggs in Barnegat
Bay, New Jersey. Environ. Res. 90, 33–39.
Burger, J., Gochfeld, M., 2000. Metal levels in feathers of 12 species of seabirds from
Midway Atoll in the northern Pacific Ocean. Sci. Total Environ. 257, 37–52.
Burger, J., Gochfeld, M., Sullivan, K., Irons, D., McKnight, A., 2008. Arsenic, cadmium,
chromium, lead, manganese, mercury, and selenium in feathers of black-legged
kittiwake (Rissa tridactyla) and black oystercatcher (Haematopus bachmani)
from Prince William Sound, Alaska. Sci. Total Environ. 398, 20–25.
Bustnes, J.O., Erikstad, K.E., Bakken, V., Mehlum, F., Skaare, J.U., 2000. Feeding
ecology and the concentration of organochlorines in Glaucous Gulls.
Ecotoxicology 9, 179–186.
Dietz, R., Sonne, C., Basu, N., Braune, B., O’Hara, T., Letcher, R.J., Scheuhammer, T.,
Andersen, M., Andreasen, C., Andriashek, D., Asmund, G., Aubail, A., Baagøe, H.,
Born, E.W., Chan, H.M., Derocher, A.E., Grandjean, P., Knott, K., Kirkegaard, M.,
Krey, A., Lunn, N., Messier, F., Obbard, M., Olsen, M.T., Ostertag, S., Peacock, E.,
Renzoni, A., Rigét, F.F., Skaare, J.U., Stern, G., Stirling, I., Taylor, M., Wiig, O.,
Wilson, S., Aars, J., 2013. What are the toxicological effects of mercury in Arctic
biota? Sci. Total Environ. 443, 775–790.
Edmonds, S., O’Driscoll, N.J., Hillier, K., Atwood, J.L., Evers, D., 2012. Factors
regulating the bioavailability of methylmercury to breeding rusty blackbirds in
northeastern wetlands. Environ. Pollut. 17, 148–154.
Frederiksen, M., Moe, B., Daunt, F., Phillips, R.A., Barrett, R.T., Bodganova, M.I.,
Boulinier, T., Chardine, J.W., Chastel, O., Chivers, L.S., Christensen-Dalsgaard, S.,
Clément-Chastel, C., Colhoun, K., Freeman, K., Gaston, A.J., Gonzalez-Solis, J.,
Goutte, A., Grémillet, D., Guilford, T., Jensen, G.H., Krasnov, I., Lorentsen, S.-H.,
Mallory, M.L., Newell, M., Olsen, B., Shaw, D., Steen, H., Strøm, H., Systad, G.H.,
Thórarinsson, T., Anker-Nilssen, T., 2012. Multi-colony tracking reveals the
winter distribution of a pelagic seabird on an ocean basin scale. Divers. Distrib.
18, 530–542.
Gaston, A.J., Hipfner, J.M., 2000. Thick-billed Murre (Uria lomvia). In: Poole, A., (Ed.),
The Birds of North America Online. Cornell Lab of Ornithology, Ithaca. Retrieved
from the Birds of North America Online: <http://bna.birds.cornell.edu/bna/
species/092> (date accessed: 03.03.15).
Gaston, A.J., Smith, P.A., Tranquilla, L., Montevecchi, W.A., Fifield, D.A., Gilchrist,
H.G., Hedd, A., Mallory, M.L., Robertson, G.J., Phillips, R.A., 2011. Movements and
wintering areas of breeding age Brünnich’s Guillemot Uria lomvia from two
colonies in Nunavut, Canada. Mar. Biol. 158, 1929–1941.
Gilchrist, H.G., Mallory, M.L., 2005. Declines in abundance and distribution
of the ivory gull (Pagophila eburnea) in Arctic Canada. Biol. Conserv. 121, 303–
309.
Ginn, H.B., Melville, D.S., 1983. Moult in Birds. BTO Guide no. 19. British Trust for
Ornithology, Tring.
Goudie, R.I., Robertson, G.J., Reed, A., 2000. Common Eider (Somateria mollissima).
In: Poole, A. (Ed.), The Birds of North America Online. Cornell Lab of Ornithology.
Retrieved from the Birds of North America, Ithaca. Online: <http://bna.
birds.cornell.edu/bna/species/546> (date accessed: 03.03.15).
GraphPad Software, Inc., 2009. InStat. GraphPad Software Inc., La Jolla, California.
Head, J.A., DeBofsky, A., Hinshaw, J., Basu, N., 2011. Retrospective analysis of
mercury content in feathers of birds collected from the state of Michigan
(1895–2007). Ecotoxicology 20, 1636–1643.
Hobson, K.A., Bond, A.L., 2012. Extending an indicator: year-round information on
seabird trophic ecology using multiple-tissue stable-isotope analyses. Mar. Ecol.
Progr. Ser. 461, 233–243.
Hobson, K.A., Sirois, J., Gloutney, M.L., 2000. Tracing nutrient allocation to
reproduction with stable isotopes: a preliminary investigation using colonial
waterbirds of Great Slave Lake. The Auk 117, 760–774.
Kidd, K., Clayden, M., Jardine, T., 2011. Bioaccumulation and biomagnification of
mercury through food webs. Environ. Chem. Toxicol. Mercury. John Wiley &
Sons Inc., pp. 453–499.
Lavoie, R.A., Jardine, T.D., Chumchal, M.M., Kidd, K.A., Campbell, L.M., 2013.
Biomagnification of mercury in aquatic food webs: a worldwide metaanalysis. Environ. Sci. Technol. 47, 13385–13394.
Lehnherr, I., St. Louis, V.L., 2009. Importance of ultraviolet radiation in the
photodemethylation of methylmercury in freshwater ecosystems. Environ.
Sci. Technol. 43, 5692–5698.
Mallory, M.L., Braune, B.M., 2012. Tracking contaminants in seabirds of Arctic
Canada: temporal and spatial insights. Mar. Pollut. Bull. 64, 1475–1484.
Mallory, M.L., Akearok, J., Edwards, D.B., O’Donovan, K., Gilbert, C.D., 2008a. Autumn
migration and wintering of northern fulmars (Fulmarus glacialis) from the
Canadian High Arctic. Polar Biol. 31, 745–750.
Mallory, M.L., Stenhouse, I.J., Gilchrist, G., Robertson, G., Haney, J.C., Macdonald, S.D.,
2008b. Ivory Gull (Pagophila eburnea). In: Poole, A. (Ed.), The Birds of North
America Online. Cornell Lab of Ornithology, Ithaca. Retrieved from the Birds of
North America Online: <http://bna.birds.cornell.edu/bna/species/175> (date
accessed: 03.03.15).
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
6
M.L. Mallory et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Mallory, M.L., Forbes, M.R., Ankney, C.D., Alisauskas, R.T., 2008c. Nutrient dynamics
and constraints on the pre-laying exodus of high Arctic northern fulmars. Aquat.
Biol. 4, 211–223.
Mallory, M.L., Allard, K.A., Braune, B.M., Gilchrist, H.G., Thomas, V.G., 2012a. New
longevity record for Ivory Gulls (Pagophila eburnea) and evidence of natal
philopatry. Arctic 65, 98–101.
Mallory, M.L., Boadway, K.A., Davis, S.E., Maftei, M.T., 2012b. Breeding biology of
Sabine’s Gull (Xema sabini) in the Canadian High Arctic. Polar Biol. 35, 335–344.
Mosbech, A., Gilchrist, G., Sonne, C., Flagstad, A., Nyegaard, H., 2006. Year-round
movements of northern common eiders Somateria mollissima borealis breeding
in Arctic Canada and West Greenland followed by satellite telemetry. Ardea 94,
651–665.
Øverjordet, I.B., Kongsrud, M.B., Gabrielsen, G.W., Berg, T., Ruus, A., Evenset, A.,
Borgå, K., Christensen, G., Jenssen, B.M., 2015. Toxic and essential elements
changed in black-legged kittiwakes (Rissa tridactyla) during their stay in an
Arctic breeding area. Sci. Total Environ. 502, 548–556.
Provencher, J.F., 2013. Parasites and pollution: why both matter to marine bird
conservation in the North. Arctic 66, 516–520.
Provencher, J.F., Mallory, M.L., Braune, B.M., Forbes, M.R., Gilchrist, H.G., 2014.
Mercury and marine birds in Arctic Canada: effects, current trends and why we
should be paying closer attention. Environ. Rev. 22, 244–255.
Robinson, S.A., Lajeunesse, M.J., Forbes, M.R., 2012. Sex differences in mercury
contamination of birds: testing multiple hypotheses with meta-analysis.
Environ. Sci. Technol. 46, 7094–7101.
Sénéchal, E., Bêty, J., Gilchrist, H.G., Hobson, K.A., Jamieson, S.E., 2011. Do purely
capital layers exist among flying birds? Evidence of exogenous contribution to
arctic-nesting common eider eggs. Oecologia 165, 593–604.
Spencer, N.C., Gilchrist, H.G., Mallory, M.L., 2014. Annual movement patterns of
endangered ivory gulls: the importance of sea ice. PLoS ONE 9 (12), e115231.
http://dx.doi.org/10.1371/journal.pone.0115231.
Tavares, S., Xavier, J.C., Phillips, R.A., Pereira, M.E., Pardal, M.A., 2013. Influence of
age, sex and breeding status on mercury accumulation patterns in the
wandering albatross Diomedea exulans. Environ. Pollut. 181, 315–320.
Thompson, D.R., Stewart, F.M., Furness, R.W., 1990. Using seabirds to monitor
mercury in marine environments: the validity of conversion ratios for tissue
comparisons. Mar. Pollut. Bull. 21, 339–342.
Thompson, D.R., Furness, R.W., Barrett, R.T., 1992a. Mercury concentrations in
seabirds from colonies in the northeast Atlantic. Arch. Environ. Contam. Toxicol.
23, 383–389.
Thompson, D.R., Furness, R.W., Walsh, P.M., 1992b. Historical changes in mercury
concentrations in the marine ecosystem of the north and north-east Atlantic
ocean as indicated by seabird feathers. J. Appl. Ecol. 29, 79–84.
Thompson, D.R., Becker, P.H., Furness, R.W., 1993. Long term changes in mercury
concentrations in herring gulls Larus argentatus and common terns Sterna
hirundo from the German North Sea coast. J. Appl. Ecol. 30, 316–320.
Thompson, D.R., Bearhop, S., Speakman, J.R., Furness, R.W., 1998. Feathers as a
means of monitoring mercury in seabirds: insights from stable isotope analysis.
Environ. Pollut. 101 (1), 93–200.
Weiser, E., Gilchrist, H.G., 2012. Glaucous Gull (Larus hyperboreus). In: Poole, A. (Ed.),
The Birds of North America Online. Cornell Lab of Ornithology, Ithaca. Retrieved
from the Birds of North America Online: <http://bna.birds.cornell.edu/bna/
species/573> (date accessed: 03.03.13).
Wolfe, M.F., Schwarzbach, S., Sulaiman, R.A., 1998. Effects of mercury on wildlife: a
comprehensive review. Environ. Toxicol. Chem. 17, 146–160.
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