Concentrations of cadmium, mercury and selenium in common eider ducks in the eastern Canadian...

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Science of the Total Environmen

Concentrations of cadmium, mercury and selenium in common

eider ducks in the eastern Canadian arctic: Influence of

reproductive stage

Mark Wayland a,*, H. Grant Gilchrist b, Ewa Neugebauer c

aEnvironment Canada, Prairie and Northern Wildlife Research Centre, 115 Perimeter Rd., Saskatoon, SK, Canada S7N 0X4bCanadian Wildlife Service, Prairie and Northern Region, Suite 301, 5204-50th St., Yellowknife, NT, Canada X1A 1E2

cEnvironment Canada, National Wildlife Research Centre, Carleton University, 1125 Colonel By Dr., Ottawa, ON, Canada K1S 5B6

Received 26 November 2004; received in revised form 23 February 2005; accepted 14 March 2005

Available online 26 August 2005

Abstract

Concentrations and total organ content of mercury, selenium and cadmium, as well as liver, kidney and body mass were

determined in female common eiders from 1997 to 2000 at the East Bay Migratory Bird Sanctuary in the eastern Canadian

arctic. In 1997 and 1999, female eiders were collected during the pre-nesting period when they eat copious amounts of food and

gain substantial weight in preparation for the rigours of nesting. In 1998 and 1999, female eiders were collected during the mid

to late stages of the nesting period when they eat very little, if at all, and, as a consequence undergo dramatic weight loss. Total

body mass, liver mass and kidney mass were highest in pre-nesting birds, especially in 1997. They were significantly lower in

nesting birds collected in 1998 and 2000. In contrast, mercury and cadmium concentrations were lowest in pre-nesting birds

collected in 1997 and 1999 and increased to significantly higher concentrations in nesting birds collected in 1998 and 2000. In

contrast to these results, the total contents of mercury in liver and cadmium in kidney did not change significantly over the 4-

year period. Hepatic selenium concentrations were relatively stable over the 4-year study period while changes in the total

content of selenium in the liver paralleled changes in liver mass and body mass. The results suggest that mercury and cadmium

concentrations in female common eiders change in response to normal changes in body and organ mass that occur during the

reproductive period. Thus, it may be important to consider body condition or reproductive stage when using common eiders

(and perhaps other species of sea ducks) in biomonitoring studies or when interpreting concentrations of metals in tissues in

terms of the risk they pose to these ducks.

Crown Copyright D 2005 Published by Elsevier B.V. All rights reserved.

Keywords: Canadian Arctic; Arctic, trace metals; Biomonitoring; Sea ducks; Common eiders; Mercury; Cadmium

0048-9697/$ - s

doi:10.1016/j.sc

* Correspondi

E-mail addre

t 351–352 (2005) 323–332

ee front matter Crown Copyright D 2005 Published by Elsevier B.V. All rights reserved.

itotenv.2005.03.033

ng author. Tel.: +1 306 975 6340; fax: +1 306 975 4089.

ss: [email protected] (M. Wayland).

M. Wayland et al. / Science of the Total Environment 351–352 (2005) 323–332324

1. Introduction

Sea ducks have been widely used as biomonitors of

inshore marine pollution in North America and Eur-

ope (Lande, 1977; Vermeer and Peakall, 1979; Karlog

et al., 1983; Di Giulio and Scanlon, 1984; Frank,

1986; Norheim, 1987; Nielsen and Dietz, 1989;

Dietz et al., 1996; Elliott and Martin, 1998; Franson

et al., 2000; Wayland et al., 2001; Barjaktarovic et al.,

2002; Savinov et al., 2003). Population declines in

several species of sea ducks have prompted further

studies to examine potential risks that contaminants,

particularly metals, pose to these birds (Henny et al.,

1995; Hoffman et al., 1998; Hollmen et al., 1998;

Stout et al., 2002; Wayland et al., 2002, 2003).

When using sea ducks in biomonitoring studies or

risk assessments, it is essential to consider attributes of

species or individuals that could influence processes

which govern contaminant levels in their tissues (Bur-

ger et al., 2003). For example, because males and

females often differ in the levels of contaminants

contained in their tissues, it is common practice to

consider only one gender or to deal with each gender

separately in biomonitoring studies and risk assess-

ments (Ohlendorf et al., 1991; Trust et al., 2000; Way-

land et al., 2001; Barjaktarovic et al., 2002; Stout et al.,

2002). Another potentially important attribute that

could affect tissue contaminant levels is body condi-

tion. For example, several studies have shown that

metal levels differ between birds that died in good

condition and those that were severely emaciated

when they died (Frank et al., 1983; Esselink et al.,

1995; Daoust et al., 1998; Debacker et al., 2000, 2001).

In several species of sea ducks, body mass and body

condition change substantially during the annual cycle

(Milne, 1976; Eadie et al., 1995; Brown and Fredrick-

son, 1997; Suydam, 2000; Jamieson, 2003). Such

changes may be important in affecting contaminant

concentrations in tissues of sea ducks. Therefore,

body condition may be an important consideration

when interpreting tissue contaminant concentrations

in biomonitoring studies or risk assessments.

The northern common eider (Somateria mollissima

borealis) is a sea duck that inhabits arctic areas of

Canada and western Greenland. Female common

eiders undergo dramatic changes in body weight and

body condition during the annual cycle (Milne, 1976;

Jamieson, 2003), especially during the pre-nesting and

nesting periods when they attain their greatest weight

and then plummet, over a period of weeks, to their

lowest weight during the year (Milne, 1976). The

purpose of this study was to determine whether con-

centrations and total organ burdens of cadmium, mer-

cury and selenium are affected by changes in body

condition that female common eiders normally expe-

rience during the breeding period. In addition, its

purpose was to explain why it is important to consider

such effects in biomonitoring programs and risk

assessments.

2. Study area and methods

2.1. Study area and sample collection

The study was conducted at the East Bay Migra-

tory Bird Sanctuary in Nunavut, Canada (64800VN�82800VW). In 1997 and 1999, female common eiders

were captured in large mist nets during the pre-nesting

period (early- to mid-June). In 1998 and 2000, female

common eiders were captured on nests during the

middle or late stages of incubation (mid- to late-

July). In 1997 and 1998, birds were killed generally

within 1 h of capture. In 1999, birds were held in

flight pens and provided food and water ad libitum for

a period of eight days, during which time they were

tested for immune function (Wayland et al., 2002). In

2000, they were held in a pen for one day after capture

for immune function testing (Wayland et al., 2003).

Following these periods in captivity, they were sacri-

ficed. The numbers of birds collected were as follows:

13 in 1997, 15 in 1998, 12 in 1999 and 21 in 2000.

Birds were weighed immediately prior to being

euthanized. Within 6 h of being euthanized, their livers

and kidneys were removed, weighed to the nearest 0.1

g, placed in acid-washed glassware and frozen.

2.2. Metals analysis

Liver and kidney samples were sent to the National

Wildlife Research Centre of Environment Canada for

analysis. Mercury and selenium were analyzed in

livers and cadmium was analyzed in kidneys. Total

mercury was analyzed by cold vapour atomic absorp-

tion spectrometry, cadmium by flame atomic absorp-

tion spectrometry and selenium by graphite furnace

M. Wayland et al. / Science of the Total Environment 351–352 (2005) 323–332 325

atomic absorption spectrometry. Analytical methods

have been described in detail by Neugebauer et al.

(2000). Percent recoveries of standard reference mate-

rials (DOLT-1 and DORM-2 from the National Re-

search Council of Canada) and spiked samples

ranged from 91% to 124% for mercury; 89% to 112%

for selenium and 92% to 108% for cadmium. Coeffi-

cients of variation (CVs) for duplicate or triplicate

analyses of samples ranged from 1% to 14% for mer-

cury; 0.2% to 8% for selenium and 0.6% to 10% for

cadmium. All metal values are reported on a dry weight

basis.

2.3. Statistics

The collection of nesting birds in two different years

and pre-nesting birds in two different years provided a

measure of replication in this study. We first examined

year-to-year differences in metal concentrations, total

metal content in organs as well as organ and bodymass.

By doing so, we were able to assess (1) whether values

of response variables were consistent between years in

which birds of a similar reproductive stage were col-

lected and (2) whether values of response variables

were consistently different among years when birds

of different reproductive stages were collected. Then,

to simplify the presentation of results, we compared

these parameters in nesting and pre-nesting birds by

combining birds from each of the 2 years in which they

were collected.

The total content of a metal in a particular organ was

calculated by multiplying the organ dry mass by the

metal concentration in the sample. Three multivariate

analyses of variance (MANOVA) were done to simul-

taneously test whether (1) metal concentrations, (2) the

total content of metals in a particular organ or (3) total

body, liver and kidney masses differed among years or

between nesting and pre-nesting birds. Significant

MANOVAs were followed by univariate analyses of

variance (ANOVA) to test whether such differences

existed for each metal (or body and organ mass),

when considered separately. For the among-year com-

parisons, significant ANOVAs were followed by mul-

tiple comparisons among means using the Tukey–

Kramer method. Raw data were log-transformed to

achieve normality and equality among variances prior

to analysis. All statistical tests were performed using

SAS software (SAS Institute, 1988).

3. Results

3.1. Among-year comparisons

Concentrations of mercury in liver and cadmium in

kidney were lower in pre-nesting birds in 1997 and

1999 than in nesting birds in 1998 and 2000 (Fig. 1A).

For mercury, the differences between 1997 and the

other years were significant (Tukey–Kramer multiple

comparison tests: P values b 0.05). Although the

mean hepatic mercury concentration of pre-nesting

birds collected in 1999 was lower than those in nest-

ing birds collected in 1998 and 2000 (Fig. 1A), the

differences were not significant (P values N 0.05).

Geometric means for mercury in Agd g�1, dry wt

(lower 95% CI–upper 95% CL) were as follows:

1997: 1.6 (1.3–2.0); 1998: 3.7 (3.2–4.4); 1999: 2.6

(2.3–2.9); 2000: 3.3 (2.6–4.2).

Renal cadmium concentrations in pre-nesting birds

collected in 1997 and 1999 were significantly lower

than those in nesting birds collected in 1998 and 2000

(Tukey–Kramer multiple comparison tests: P values b

0.05), while the differences between pre-nesting birds

in 1997 and 1999 and between nesting birds in 1998

and 2000 were not significant (P values N 0.05).

Geometric means and confidence limits for cadmium

were as follows: 1997: 68 (58–80); 1998: 163 (140–

190); 1999: 81 (55–120) and 2000: 165 (138–192).

Hepatic selenium concentrations did not differ sig-

nificantly among years (ANOVA: P=0.28). Geometric

means and confidence intervals for selenium were as

follows: 1997: 19.4 (15.5–24.3); 1998: 17.3 (14.2–

20.9); 1999: 14.1 (11.2–17.7); 2000: 16.1 (12.8–20.4).

The results of analyses that examined inter-annual

variation in the total organ content of the different

metals were generally opposite to the results reported

above for concentrations of metals (Fig. 1B). Hepatic

mercury and renal cadmium content did not differ

significantly among years (ANOVA for mercury:

P=0.051; ANOVA for cadmium: P=0.49), although

the difference between 1998 and 1999 for hepatic

mercury was nearly significant. In contrast, total he-

patic selenium content differed significantly among

years (ANOVA: P b0.001). Pre-nesting birds collect-

ed in 1997 had significantly more selenium in their

livers than their counterparts collected in 1999 or

nesting birds collected in 1998 and 2000 (P values

b 0.05), while pre-nesting birds collected in 1999 had

PN INC PN INC1997 1998 1999 2000S

e &

Hg

Co

nce

ntr

atio

ns

(µg

/g d

ry w

t)

1

10

20

50

Cd

Co

nce

ntr

atio

n (

µg/g

dry

wt)

1

30

100

300

A

B

1997 1998 1999 2000

Se

& H

g C

on

ten

t in

live

r (µ

g)

1

30

50

100

200

500

Cd

Co

nte

nt

in k

idn

eys

(µg

)

1

50

100

300

700

PN INC PN INC

Selenium Mercury Cadmium

B

Fig. 1. (A) Geometric mean (F 95% CI) hepatic concentrations of mercury and selenium and renal concentrations of cadmium (Agd g�1 dry

wt) in pre-nesting (PN) female common eiders in 1997 and 1999 and in nesting (INC) female common eiders in 1998 and 2000. (B)

Geometric mean (F 95% CI) total hepatic content of mercury and selenium and renal content of cadmium (Ag) in female common eiders as

described in (A).


significantly more selenium in their livers than nesting

birds collected in 2000 (P b0.05). The differences

between selenium content in pre-nesting birds collect-

ed in 1999 and nesting birds collected in 2000 and

between nesting birds collected in 1998 and 2000

were not significant (P values N 0.05).

Body, liver and kidney mass were greatest in pre-

nesting birds in 1997, were somewhat lower in pre-

nesting birds collected in 1999 and were lowest in

nesting birds collected in 1998 and 2000 (Fig. 2).

The differences in body and organ masses between

1997 and all other years were significant (P values b

0.05). In addition, body, liver and kidney masses of

pre-nesting birds collected in 1999 were greater

than in nesting birds collected in 1998 and 2000

(P values b 0.05). Liver mass did not differ sig-

nificantly between nesting birds collected in 1998

and those collected in 2000 (P N0.05). However,

kidney and body masses of nesting birds collected

in 2000 were slightly but significantly higher than

those of their counterparts collected in 1998 (Fig. 1B, P

values b 0.05).

Table 1

Geometric means and confidence limits for concentrations (Agd g�1

dry wt) and total organ content (Ag) of cadmium, mercury and

selenium as well as liver, kidney and body mass (g wet wt) in

nesting and pre-nesting female common eider combined across

years in which each of these groups of birds was collected (pre-

nesting birds collected in 1997 and 1999 and nesting birds collected

in 1998 and 2000)

Parameter Pre-nesting (n =25) Nesting (n =36)

Cd concentration 74 (61–90) 164 (146–184)

Hg concentration 2.0 (1.7–2.4) 3.5 (3.0–4.0)

Se concentration 16.6 (14.2–19.6) 16.6 (14.3–19.3)

Cd content in kidneys 388 (329–457) 436 (392–483)

Hg content in liver 34 (30–40) 26 (23–30)

Se content in liver 282 (225–353) 124 (106–146)

Liver mass 56.6 (52.1–61.6) 26.2 (24.9–27.6)

Kidney mass 20.7 (19.5–22.0) 11.8 (11.2–12.5)

Body mass 1867 (1765–1976) 1376 (1322–1431)

B

1997 1998 1999 2000

Liv

er /

Kid

ney

s W

t (g

)

1

10

100

To

tal B

od

y W

t (g

)

1000

1500

2000

2500

3000

PN INC PN INC

Liver Kidneys Total Body

Fig. 2. Geometric mean (F 95% CI) body, liver and kidney mass (g wet wt) in pre-nesting (PN) female common eiders in 1997 and 1999 and in

nesting (INC) female common eiders in 1998 and 2000.


3.2. Comparisons of pre-nesting and nesting birds

combined across years

Pre-nesting birds from both years (1997 and 1999

combined) had significantly lower concentrations of

mercury and cadmium than their nesting counterparts

from both years (1998 and 2000) (P values b 0.0001;

Table 1). Selenium concentrations did not differ be-

tween pre-nesting and nesting birds combined from

both years (P=0.98; Table 1).

Cadmium content in kidneys of pre-nesting birds

(1997 and 1999 combined) did not differ significantly

from that of nesting birds (1998 and 2000 combined)

(P=0.21; Table 1). However, total hepatic content of

mercury (P=0.009) and selenium (P b0.0001) were

greater in pre-nesting birds than in nesting birds.

Mean hepatic mercury and selenium contents were

approximately 1.3 and 2.3 times greater, respectively,

in pre-nesting birds than in nesting birds (Table 1).

Liver, kidney and body mass were significantly

greater in pre-nesting birds (1997 and 1999 combined)

than in nesting birds (1998 and 2000 combined) (P

values b 0.0001). Mean liver, kidney and body mass

were about 2.2, 1.8 and 1.3 times greater, respectively,

in pre-nesting birds than in nesting birds (Table 1).

Over all years, cadmium concentrations were sig-

nificantly and inversely correlated with kidney mass

(rpearson=� 0.76, P b0.001, Fig. 3) and body mass

(rpearson=� 0.64, P b0.0001. Similarly, mercury con-

centrations were significantly and inversely correlated

with liver mass (rpearson=� 0.57, P b0.0001, Fig. 3)

and body mass (rpearson=� 0.71, P b0.0001). In con-

trast, selenium concentrations were not significantly

correlated with liver mass (rpearson=0.08, P=0.53,

Fig. 3) or body mass (rpearson=0.16, P=0.22). How-

ever, the total content of selenium in liver was signifi-

cantly correlated with liver mass (rpearson=0.73, P b

0.0001) and body mass (rpearson=0.66, P b0.0001).

20 50 100

Se

Co

nce

ntr

atio

n (

µg/g

dry

wt)

5

10

20

50

100

Liver Wt (g)

20 50 100

Hg

Co

nce

ntr

atio

n (

µg/g

dry

wt)

1

2

5

10

Kidney Wt (g)

7 10 20 40

Cd

Co

nce

ntr

atio

n (

µg/g

dry

wt)

40

100

200

300

400

A

B

C

rpearson = 0.081, p=0.53

rpearson = -0.57, p<0.0001

rpearson = -0.76, p<0.0001

1997199819992000

Fig. 3. Correlations between liver mass (g) and hepatic selenium (A) and mercury (B) concentrations (Agd g�1) and kidney mass (g) and renal

cadmium concentrations (Agd g�1) (C) in female common eiders over the period 1997–2000.



4. Discussion

One potential shortcoming of this study was that

pre-nesting and nesting birds were not sampled in the

same year and some between-year variability is likely

to occur irrespective of reproductive status. This in-

deed appeared to be the case for total hepatic mercury

content and organ and body mass. Despite this short-

coming, the replication of sample collections of each

group of birds over 2 years demonstrated that mercury

and cadmium concentrations varied in relation to

reproductive stage and body condition. In contrast,

selenium concentrations, but not total hepatic content

of selenium, did not vary according to reproductive

stage and body condition.

Female common eiders undergo dramatic changes

in body condition between the pre-nesting and nesting

periods. During the pre-nesting period, female eiders

eat copious amounts of food, gain weight and increase

their fat stores as they prepare for the rigours of

nesting (Milne, 1976; Korschgen, 1977; Parker and

Holm, 1990). In contrast, during the nesting period,

they eat very little, if at all, as they spend nearly all of

their time incubating eggs and protecting their nests

from predators (Korschgen, 1977; Bolduc and Guil-

lemette, 2003). As a result, their body mass and body

condition decrease substantially during the nesting

period (Korschgen, 1977; Parker and Holm, 1990;

Bolduc and Guillemette, 2003). Our results were con-

sistent with findings reported in the studies cited

above. Pre-nesting female common eiders were heavi-

er and had larger livers and kidneys than nesting

eiders.

In this study, hepatic mercury and renal cadmium

concentrations were higher in the lighter, nesting birds

sampled in 1998 and 2000 than in the heavier, pre-

nesting birds sampled in 1997 and 1999. In contrast,

the total content of mercury in the liver and cadmium

in kidneys did not change significantly among years

(although for mercury, variation among years was

nearly significant). Esselink et al. (1995) reported

similar results for copper and iron in a sample of

barn owls that varied widely in body condition and

concluded that seasonal changes in physiology affect

metal concentrations in animal tissues. Stewart et al.

(1994) reported that cadmium and mercury concentra-

tions in common guillemots (Uria aalge) varied sea-

sonally in part due to lipid and protein mobilization

during reproduction. However, the seasonal changes

they documented were not apparently related to

changes in body and organ mass, but rather to phys-

iological changes which involved the uptake of nutri-

ents and non-essential metals (Stewart et al., 1994).

Several studies have shown that certain metals are

often found in higher concentrations in livers or

kidneys of extremely emaciated birds when compared

to birds in good body condition (Frank et al., 1983;

Esselink et al., 1995; Debacker et al., 2000; Daoust et

al., 1998). However, there are few reports of seasonal

changes in metal concentrations that appear to be

linked primarily to normal seasonal changes in overall

body mass or the mass of various organs. One such

study showed that renal and hepatic cadmium con-

centrations in reindeer were at their lowest at a time of

year when body mass, liver mass and kidney mass

were reaching their peak (Borch-Iohnsen et al., 1996).

In that study, the total content of cadmium in liver and

kidneys changed little over the course of the year.

Another study (Osborn, 1979) showed that hepatic

concentrations of cadmium, copper and zinc peaked

immediately prior to moult in starlings and coincided

with the time of year when liver mass was at its

lowest, mainly due to the depletion of fat in the

liver. Fluctuations in lipid mass in organs associated

with reproductive stage may explain the changes we

observed in mercury and cadmium concentrations and

the absence of changes we observed in the organ

content of these metals. As fat reserves are depleted,

tissue mass declines while the pool of mercury and

cadmium remains relatively unaffected since these

metals are bound to proteins, not lipids. The result

is an increase in mercury and cadmium concentration

with little change in content. We did not measure lipid

concentrations in organs but observed that, in general,

pre-nesting birds had substantially larger fat reserves

than nesting birds (Wayland et al., 2002, 2003). Our

results reported in these earlier papers agree with the

results from other studies, which showed that lipid

reserves in female common eiders declined markedly

from the pre-nesting to mid- or late-nesting periods

(Milne, 1976; Korschgen, 1977; Parker and Holm,

1990).

In contrast to mercury and cadmium, hepatic sele-

nium concentrations did not vary with year. However,

the content of selenium in liver was generally lower in

nesting birds sampled in 1998 and 2000 than in pre-


nesting birds sampled in 1997 and 1999. In contrast to

mercury and cadmium, which are non-essential ele-

ments, selenium is an essential nutrient which is

physiologically regulated to meet nutritional needs

(Daniels, 1996). The depletion of selenium in fasting

eiders during the nesting period paralleled the de-

crease in liver mass that occurred during that period.

The liver is involved in the metabolism of selenium

and the content of selenium in the liver likely reflects

overall selenium status (Daniels, 1996). Thus, in fast-

ing animals such as female common eiders during the

nesting period, the decrease in hepatic selenium con-

tent likely reflects an overall decrease in selenium

status as selenium reserves are metabolized and used

to meet nutritional needs. Consistent with our results,

Rattner and Jehl (1997) reported that seasonal changes

in hepatic selenium content mirrored changes in liver

mass of eared grebes (Podiceps nigicollis). Similarly,

while hepatic concentrations of selenium did not

change substantially in reindeer over several seasons,

seasonal changes in total content of selenium in their

livers paralleled changes in liver mass (Borch-Iohnsen

et al., 1996).

We found that mercury and cadmium concentra-

tions were inversely correlated with liver mass, kid-

ney mass and body mass over the 4-year period. In

earlier papers, we reported that concentrations of

these metals were inversely correlated with various

body condition indices (Wayland et al., 2001, 2002,

2003). Our results were similar to those reported in

other field studies of sea ducks wherein concentra-

tions of various metals were inversely correlated

with body weight or the mass of various organs

(Henny et al., 1991; Ohlendorf et al., 1991; Hoffman

et al., 1998; Franson et al., 2000). It has been

postulated that exposure to metals may contribute

to poor body condition in ducks (Takekawa et al.,

2002). However in earlier papers, we noted that

experiments in which captive birds were orally

dosed with cadmium and mercury did not find a

relationship between metal exposure and body con-

dition and cautioned that the inverse correlations

between metal concentrations and body condition

in field studies of sea ducks may not be the result

of a cause and effect relationship (Wayland et al.,

2002, 2003). The lack of agreement between the

results of field and captive studies prompted us to

suggest a need for further studies to resolve this

conundrum. We believe that the results of this

study offer some insight into the lack of agreement

between laboratory and field studies examining metal

levels and their effects on sea ducks. In simple

terms, cadmium and mercury concentrations are like-

ly to fluctuate seasonally, in response to normal

patterns of weight gain and loss, especially as they

are related to the acquisition and depletion of fat

reserves. Thus, it is important to consider body

condition when conducting biomonitoring studies in

which sea ducks are used and when assessing the

risks that exposure to metals may pose to sea ducks.

Failure to account for the relationship between body

condition and metal levels in eiders (and possibly

other species of birds as well) could lead researchers

to conclude erroneously, that a particular group of

birds with relatively high metal levels is at greater

risk than other groups of birds with lower metal

levels, when the difference between the two groups

may simply be due to differences in body condition.

Acknowledgements

We thank the following individuals who assisted in

various phases of this study: K. Allard, T. Armstrong,

G. Bottitta, P. Dunlop, C. James, S. Jamieson, R.

McNeil, J. Nakoolak, G. Savard, and K. Timm. Fund-

ing was provided by Environment Canada (Prairie and

Northern Region), the Department of Indian Affairs

and Northern Development through their Northern

Contaminants Program and the Government of Cana-

da’s Toxic Substances Research Initiative. Animals

were collected under scientific permits issued by the

Canadian Wildlife Service and the Government of

Nunavut and according to procedures approved by

the University of Saskatchewan Animal Care Com-

mittee acting on behalf of the Canadian Council of

Animal Care.

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