EcoHealth 9, 267–277, 2012

DOI: 10.1007/s10393-012-0784-4

Ó 2012 International Association for Ecology and Health

Original Contribution

Mercury Concentrations in Hair from Neonatal and Juvenile

Steller Sea Lions (Eumetopias jubatus): Implications Based
on Age and Region in this Northern Pacific Marine Sentinel
Piscivore

J. Margaret Castellini,1 Lorrie D. Rea,2 Camilla L. Lieske,3 Kimberlee B. Beckmen,2 Brian S. Fadely,4
John M. Maniscalco,1,5 and Todd M. O’Hara3,6
1
Institute of Marine Science, School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 905 N. Koyukuk Drive, 245 O’Neill Building,
P.O. Box 757220, Fairbanks, AK 99775-7220
2
Division of Wildlife Conservation, Alaska Department of Fish and Game, 1300 College Rd, Fairbanks, AK 99701-1551
3
Institute of Arctic Biology, University of Alaska Fairbanks, 311 Irving I, Fairbanks, AK 99775
4
National Marine Mammal Laboratory, Alaska Fisheries Science Center, NOAA Fisheries, 7600 Sand Point Way N.E, Seattle, WA 98115
5
Alaska SeaLife Center, 301 Railway Avenue, P.O. Box 1329, Seward, AK 99664
6
Department of Biology and Wildlife, College of Natural Science and Mathematics, University of Alaska Fairbanks, 211 Irving I, Fairbanks, AK 99775

Abstract: Mercury is a global contaminant of concern for the fetus and the neonate of piscivores. Methyl-
mercury, produced within marine ecosystems, is of particular concern as a readily absorbed neurotoxicant
transported across the blood brain barrier and transplacentally. In the North Pacific Ocean, Steller sea lions are
broadly distributed apex predators and, as such, integrate complex food webs and the associated exposure and
possible adverse effects of toxic and infectious agents. Hair, including lanugo, was examined using regional and
age groupings to assess mercury concentrations in young Alaskan Steller sea lions. The highest concentrations
of mercury occurred in the youngest animals, likely via in utero exposure. Based on the adverse developmental
outcomes of methylmercury toxicity this specific cohort is of concern. Regionally, higher concentrations of
mercury were observed in the endangered western population of Steller sea lions and mirrored patterns
observed in human biomonitoring studies of Alaskan coastal communities. These data have broader impli-
cations with respect to human and ecosystem health as Steller sea lions rely on similar prey species and foraging
areas as those targeted by commercial fisheries and subsistence users and are therefore valuable sentinels of
marine ecosystem health.

Keywords: mercury, methylmercury, hair, neonate, pup, marine sentinel, Steller sea lion, toxicology,
ecotoxicology, ecosystem health

INTRODUCTION
Marine mammals are important sentinels of change in the
Published online: July 20, 2012 marine environment (Gulland 1999; Reddy et al. 2001;
Correspondence to: J. Margaret Castellini, e-mail: maggie.c@alaska.edu Aguirre and Tabor 2004; Bossart 2006; Kirk et al. 2010a, b;
268 J. Margaret Castellini et al.
Knott et al. 2011). In Alaska, declining Steller sea lion
(Eumetopias jubatus, SSL) populations (Merrick et al. 1987;
Loughlin et al. 1992) accompanied by declines in other
marine mammal and bird populations (National Research
Council 1996; Merrick 1997) have signaled major shifts in
ecosystem structure and health that may have roots in a
number of factors, both natural and anthropogenic
(Anderson and Piatt 1999; Trites et al. 1999; DeMaster et al.
2006). In 1997, the National Marine Fisheries Service
(NMFS) of the United States recognized two genetically
distinct population segments (DPS) of SSLs and, under the
US Endangered Species Act, listed the western DPS (west of
144°W longitude) as endangered and retained the listing of
threatened for the eastern DPS (east of 144°W longitude)
(NMFS 1997). Population trends are variable within these
broader geographic areas, including both regions of growth
and decline, complicating analysis of spatial and temporal
changes (Fritz and Gelatt 2010; Mathews et al. 2011). De-
spite intensive research, the causes of the population de-
cline and inconsistent recovery remain uncertain and are
likely a combination of effects resulting from a changing
environment (Loughlin 1998; Trites and Donnelly 2003;
Springer et al. 2003; Burek et al. 2005; NMFS 2008).
Through diet, Steller sea lions integrate the effects of
toxic and infectious agents from complex food webs. Their
prey base and foraging areas overlap in the Northern Pacific
with commercial and subsistence fisheries for species such
as walleye pollock (Theragra chalcogramma), Pacific cod
(Gadus macrocephalus), Atka mackerel (Pleurogrammus
monopterygius), and salmonids (Oncorhynchus sp.) (Sinclair
and Zeppelin 2002). Thus, the dietary needs of pinnipeds
and humans are linked as are the associated exposure and
possible adverse effects of toxic and infectious agents within
the marine ecosystem. This shared ecosystem is experi-
encing increased marine traffic and resource development
and is vulnerable to regime shifts, warming, and ocean
acidification (NMFS 2008). These environmental stressors
can impact exposure and biological responses to toxic and
infectious agents (Aguirre and Tabor 2004).
Among the potential factors affecting SSL populations,
exposure to contaminants is a topic of concern (NMFS
2008). Previous studies have indicated that SSLs from the
western endangered DPS might face greater exposure to
mercury than those in the eastern DPS (Beckmen et al.
2002; Holmes et al. 2008). Methylmercury (MeHg) expo-
sure in SSLs is mostly dietary resulting from bioaccumu-
lation and biomagnification (Beckmen et al. 2002; Wiener
et al. 2003) with an unknown amount of anthropogenic
contribution (Dietz et al. 2011a, b). Chronic exposure at
low concentrations can cause subtle adverse effects, par-
ticularly on the developing brain (Grandjean et al. 1997;
Castoldi et al. 2001; Oken et al. 2005; Basu et al. 2009).
Methylmercury can also have deleterious effects on many
organ systems and laboratory studies have suggested syn-
ergistic effects among mercury and other contaminants
known to occur in SSLs (Burbacher et al. 1990; Bemis and
Seegal 1999; Beckmen et al. 2002; Holmes et al. 2008).
Methylmercury is readily absorbed and transported across
the blood brain barrier and transplacentally (Jones et al.
1976; Wagemann et al. 1988; Clarkson 1994). Therefore,
the central nervous system of fetuses and neonates is of
concern with respect to MeHg toxicity.
Hair is a suitable matrix for assessing MeHg exposure
using total mercury concentration ([THg]) (Davidson et al.
2006, 2008). This study examines, with much finer tem-
poral and spatial resolution than previously, regional-
and age-related exposure to mercury in Alaskan SSLs.
This approach allows for a more complete assessment of
MeHg exposure for the cohorts of greatest concern (fetus
and neonate). These data have broader implications with
respect to human and ecosystem health as SSLs rely on
similar prey species and foraging areas as those targeted by
commercial fisheries and subsistence users. Steller sea lions
therefore function as valuable sentinels of marine ecosys-
tem health.
METHODS
Sample Collection
Two hundred and fifty-six hair samples were collected from
SSLs during live capture/release studies conducted from 1998
to 2009. Sea lions between 2 weeks and 38.5 months of age
were captured at haulouts and rookeries in Southeast Alaska
(SEA; n = 97), Prince William Sound (PWS; n = 100), the
central Gulf of Alaska (CGOA; n = 23), and the central and
eastern Aleutian Islands (AI; n = 36) (Fig. 1).
Body mass was measured using a hanging scale (±0.1 kg)
(TCI Scales Inc, Ocean King D-6, Snohomish, WA, USA or
Rice Lake Weighing Systems, IQ Plus 390-DC, Rice Lake, WI,
USA). Age was estimated by the date of capture [assuming a
mid-June birth date (Pitcher et al. 2001)], and color or con-
sistency of the pelage, and confirmed using measurements of
the canine tooth and diastema (King et al. 2007). Hair was
collected from a 2 9 2 cm patch of skin just forward of the
 Mercury Concentrations in Steller Sea Lion Hair 269

Figure 1. Sampling regions for

Alaskan Steller sea lions (E. juba-
tus). 144°W represents the geo-
graphical demarcation between
the western (AI central and east-
ern Aleutian Islands, CGOA cen-
tral Gulf of Alaska, PWS Prince
William Sound), and eastern
(SEA southeast Alaska) DPS.

insertion of the pelvic flipper on the right side using surgical rials in each measurement run. Recoveries were
scissors or grooming shears. Hair was cut close to the skin and 99.6 ± 2.1% (1 lg/g standard), 88.3 ± 5.4% (IAEA 086,
stored in polypropylene bags at ambient temperature until human hair), and 96.6 ± 2.1% (IAEA 085, human hair
processing for analysis. spiked with MeHg).

Mercury Analysis
Hair samples were grouped according to age and region Table 1. Year of Capture and Sample Size for Each Age Class of
Steller Sea Lion (E. jubatus) According to Region. SEA (Southeast
(Table 1). Age groups reflect specific developmental stages:
Alaska), PWS (Prince William Sound), CGOA (Central Gulf of
young pups (3 months, pre-molt with lanugo that rep-
Alaska), AI (Central and Eastern Aleutian Islands)
resents in utero growth), old pups (*5 months, combi-
nation pre- and post-molt with hair that may represent a Age class Regions
milk diet), young of the year (YoY, 7–10 months, post-
Sea PWS CGOA AI
molt with hair that represents a mostly milk diet), yearlings
(12–23 months, transition to independent piscivory), and Years n Years n Years n Years n
juveniles (24–38.5 months, typically fully weaned). Re- Young pup (<3 months) 2000 10 2000 12 2008 12 2008 12
gional groups include one from the eastern DPS (threa- 2008 16
tened; SEA) and three from the western DPS (endangered; Old pup (*5 months) 1998 12 2001 21
PWS, CGOA, and AI) (Fig. 1). 2002 12
Prior to analysis, hair samples were washed with 1% 2009 24
TritonTM X-100, rinsed with milliQ water and air-dried or, YoY (7.5–10 months) 2000 6 2006 16 2001 11 2003 7
in later samples (2009), freeze-dried (Airey 1983). Total 2008 15 2005 17
mercury concentration was measured using a Milestone Yearling (12–23 months) 2000 20 2000 16
DMA80 Direct Mercury Analyzer (US EPA method 7473) 2009 7
Juvenile (24–38.5 months) 2001 2 2000 1
(Knott et al. 2011). Quality control included a 1 lg/g cal-
2004 4 2002 3
ibration standard and IAEA hair standard reference mate-
270 J. Margaret Castellini et al.

Statistical Analyses RESULTS

Comparison of [THg] in air- and freeze-dried hair was
Prince William Sound and SEA were the only regions from
conducted using 15 samples collected in 2008 and ana-
which hair samples were collected from all age classes
lyzed in 2009. These were subsampled and reanalyzed as
(Fig. 2). Young pups in both locations had higher [THg]
both air- and freeze-dried samples. Because [THg] was
than most older groups captured in the same location
normally distributed, differences among [THg] (original
(Kruskal–Wallis all pairwise comparison, P < 0.005). In
air-dried, reanalyzed air-dried, and reanalyzed freeze-
SEA, there was no significant difference between [THg] in
dried) were evaluated using a two-way randomized block
young pups and juveniles; however, both groups had sig-
analysis (blocked by individual SSL) with Tukey’s multiple
nificantly higher concentrations than the other age classes
comparison. No significant difference was found between
(old pup, YoY, and yearling). In PWS, young pups had
[THg] of original and reanalyzed air-dried samples, while
significantly higher [THg] than all other age classes. In
those that had been freeze-dried were significantly higher
addition, [THg] was significantly higher in old pups than
(P < 0.0001) than air-dried samples by 8.0 ± 6.6%. For
YoY in PWS. These observations are consistent with results
regions and age groups that included both air and freeze-
when only data from 2000 were analyzed (eliminating any
dried hair, the range of individual values was 8% (RSD
multi-year or sample processing differences). In 2000,
61–67%) and there were no significant differences be-
young pups from SEA and PWS had significantly higher
tween years represented by the different treatments within
[THg] than other age classes from their region although
a region. As freeze-dried samples did not impact com-
not all age classes are represented (Table 2).
parisons by region, they were included in further analyses.
Comparing young pups regionally, [THg] was signifi-
Interannual [THg] variability was assessed using a
cantly higher in pup hair from PWS, CGOA, and AI
Kruskal–Wallis test with Conover-Inman multiple com-
(8.26 ± 5.5, 8.24 ± 3.77, 7.74 ± 2.71 lg/g, respectively;
parison, testing for differences in region and year for all age
western DPS) compared to SEA (4.09 ± 1.62 lg/g; eastern
groups separately. Within a given region no differences
DPS) (Fig. 3a). These differences persisted when concen-
among years was noted for young pups, yearlings, or
trations were expressed on a body mass-specific basis
juveniles. For those regions where significant differences
(Fig. 3b) or when only data from a single year (2000; PWS
among years occurred (P < 0.05; old pups and YoY), the
and SEA) were included in the analyses. There were no
ranges and confidence intervals for the different years
overlapped and it was determined that pooling by year
would not significantly impact the other comparisons.
For regional comparisons of both mean [THg] and
body mass-specific mean [THg], differences among the
mean ranks of the four groups were tested for using a
Kruskal–Wallis test, with Conover-Inman pairwise com-
parisons if global significance was detected. Differences in
the variance among the four groups were tested for using
squared ranks approximate equality of variance with pair-
wise comparisons if global significance was detected. For
age comparisons within SEA and PWS, differences among
mean ranks for [THg] were tested using a Kruskal–Wallis
test, with Conover-Inman pairwise comparisons. Young
pups were omitted from the analysis if they were described
Figure 2. Box and whisker plot of hair [THg] for young pups (<3-
as having any evidence of molt beginning. month old), old pups (*5-month old), YoY (7- to 10-month old),
Statistical analyses were done using StatsDirect yearlings (12- to 23-month old) and juveniles (24- to 38.5-month
version 2.7.8 (Tidestone Technologies Inc.) and Minitab old) from SEA and PWS. Horizontal line median, boxes the mid 50%
version 15.1.1 (Minitab Inc.) statistical software and, unless distribution, whiskers the upper and lower 25% and individual points
otherwise noted, P values <0.05 were considered signifi- represent outliers. The width of each bar is proportional to the
cant. sample size (Table 1).
 Mercury Concentrations in Steller Sea Lion Hair 271

Table 2. Total Mercury Concentration ([THg]; lg/g) in Steller

Sea Lion (E. jubatus) Hair from Different Age Classes from 2
Regions in Alaska—Prince William Sound (PWS; Western
Endangered DPS) and Southeast Alaska (SEA; Eastern Threatened
DPS) Collected in 2000

Young pup YoY Yearling

2- to 3-month- 7.5- to 10- 12- to 23-
old pre-molt, month-old month-old
suckling post-molt, combination
suckling
SEA b c c
Mean ± SD 4.09 ± 1.62 1.57 ± 0.58 1.64 ± 0.87
Range 2.20–6.38 0.97–2.61 0.77–3.95
n 10 6 20
PWS a c
Mean ± SD 9.09 ± 6.30 1.78 ± 0.80
Range 1.30–21.26 0.91–3.37
n 12 16

Significant differences (Kruskal–Wallis test, with Conover-Inman pairwise

comparisons, P < 0.05) are represented by different lower case letters,
a>b>c

statistical differences among the pups from the western

DPS groups which had a high degree of variability within Figure 3. Box and whisker plot of hair [THg] (A) and body mass-
each group. Three PWS pups had hair [THg] > 20 lg/g. specific [THg] (B) in young pups (<3-month old) and YoY (7- to
10-month old) from 4 regions in Alaska. AI, CGOA, and PWS
Variance in [THg] among the pups from the western DPS
represent the western DPS (endangered), SEA represents the eastern
groups was not different, while variance in [THg] between
DPS (threatened). Horizontal line median, boxes the mid 50%
the eastern DPS and each group within the western DPS
distribution, whiskers represent the upper and lower 25% and
was significantly different. In contrast to young pups, YoY
individual points represent outliers. Significant differences (Kruskal–
from all locations had relatively low hair [THg]. Although Wallis test, with Conover-Inman pairwise comparisons, P < 0.05)
there were significant differences in hair [THg] (Fig. 3a) are represented by different lower case letters.
and in body mass-specific hair [THg] (Fig. 3b) among re-
gions, there were no differences in variance detected
higher than the 10–20 lg/g maternal hair threshold range
(P = 0.1; squared ranks approximate equality of variance)
established by the World Health Organization (WHO
and the 95% confidence interval for all regions overlapped.
1990) for which fetal neurological effects might be expected
Comparisons were made between hair [THg] in young
in humans. Four individuals from the western DPS had
pups and selected reported wildlife thresholds and human
[THg] above the Agency for Toxic Substances and Disease
thresholds that have been established by various biomoni-
Registry (Risher and DeWoskin 1999) threshold value of
toring programs for women of childbearing age (Fig. 4).
15.3 lg/g (maternal hair), including the 10% of young
Within the western DPS 50–67% of SSL hair samples from
pups from PWS for which hair [THg] was above 20 lg/g.
young pups were above both the human threshold estab-
lished by the Alaska Hair Mercury Biomonitoring Program
(AHMBP; State of Alaska Epidemiology Bulletin 2010) DISCUSSION
and one suggested for subclinical effects in polar bears
(Dietz et al. 2011b), compared to 10% from SEA. One- Hair is an excretory route for MeHg in mammals and
third (33–36%) of young pups sampled from each of the commonly used for biomonitoring human populations
three western DPS regions had [THg] values within or (Davidson et al. 2006, 2008). Steller sea lions undergo a
272 J. Margaret Castellini et al.
Figure 4. Total mercury concentration ([THg]; (lg/g)) in hair from
young Steller sea lion (E. jubatus) pups (<3-month old) from four
regions in Alaska compared to several published health-related
thresholds for hair [THg] in other wildlife and humans, presented
number of physiological and nutritional changes through
their first 2 years that affect [THg] in hair either because of
differences in routes of exposure (i.e., in utero exposure,
dietary exposure through milk, transition from milk to
independent piscivory) or via molt status. With more SSL
samples available for analysis in this study than in previous
investigations (Beckmen et al. 2002; Holmes et al. 2008), it
was possible to refine cohort designations with respect to
MeHg exposure within critical developmental periods by
distinguishing three separate age classes within the first year
as well as yearlings and juveniles.
In both PWS and SEA, hair from young pups (lanugo,
representative of in utero exposure) had significantly higher
[THg] compared to that of most age classes examined
(Fig. 2). Pups from the old pup and YoY age classes
(molting and post-molt) had lower [THg], representative
of dietary exposure through milk. Yearling concentrations
remained low as some continued to depend nutritionally
on suckling while others transitioned to independent for-
aging (Rea et al. 2011). Concentrations began to increase in
independently foraging juveniles. Similar results were ob-
served when only data from 2000 were considered, which
included fewer age categories but eliminated potential
interannual or sample processing variability (Table 2).
These results are consistent with expected routes of expo-
sure during development. Methylmercury is transported
transplacentally, so maternal MeHg associated with a high
trophic level marine diet can be transferred to the devel-
for context. AI, CGOA, and PWS represent the western DPS
(endangered), SEA represents the eastern DPS (threatened). 1Thomp-
son 1996; 2Risher and DeWoskin 1999; 3WHO 1990; 4Dietz et al.
2011b; 5State of Alaska Epidemiology Bulletin 2010.
oping fetus (Wagemann et al. 1988). While MeHg may be
present at low levels in milk, it is not usually the main route
of exposure for neonates (Oskarsson et al. 1995, 1998). The
high [THg] observed in lanugo are of particular concern as
they suggest that some SSL pups encounter significant
exposure to mercury in utero, a critical developmental
period.
In addition to considering molt and nutritional status,
potential regional differences in [THg] between the western
and eastern DPSs were examined. Previous studies have
reported higher [THg] in SSL pups from PWS than from
SEA (Beckmen et al. 2002; Holmes et al. 2008). In both
cases, SSLs were classified as pups if they were less than
1-year old. As there can be very large differences in [THg]
at different ages within the first year, it is important to use
more narrowly defined age classifications to validate pre-
viously reported regional differences. In this study, young
pups from all three groups within the western DPS,
including PWS, had significantly higher and more variable
hair [THg] than did similarly aged pups from SEA
(Fig. 3a), consistent with results reported by Beckmen et al.
(2002). Conversely, while there were statistically significant
differences in [THg] among regions in YoY, concentrations
were relatively low overall, the 95% confidence interval for
all regions overlapped, and the differences were minor from
a toxicological perspective. In regions where data were
available there was little evidence of interannual varia-
tion—even when significant differences were evident (old

pups and YoY) the ranges and confidence intervals over-
lapped. There was no significant difference between 2000
and 2008 in young pups from PWS. Regional differences in
[THg] do not appear to be directly correlated to recent
population trends in those areas. During the sampling
period of this study (1998–2009) all sampled regions
showed increases in pup production, with a greater annual
rate of increase at rookeries in the eastern Gulf of Alaska
(including Prince William Sound) than in Southeast Alaska
(Fritz and Gelatt 2010).
Calculating hair [THg] on a body mass-specific basis did
not affect regional differences (Fig. 3b). This was done to as-
sess whether differences in mass within an age group (e.g.,
growth dilution) might contribute to regional differences in
hair [THg]. The potential for growth dilution within young
pups is limited by the possibility that lanugo does not continue
to grow markedly after birth (Ashwell-Erickson et al. 1986)
and is likely more related to growth during fetal development.
The issue of growth dilution may be more important when
considering [THg] differences among young pups and older
pups, YoY, yearlings, and juveniles.
There appears to be greater variability in fetal exposure in
much of the western DPS of SSLs compared to the eastern
DPS. Fetal exposure to MeHg can result in impaired neuro-
logical development. In humans, fetal exposure has been
shown to impact cognitive development, memory, attention,
language, fine motor, and visual spatial skills (Davidson et al.
2006). In the Faroe Islands, where fetal MeHg exposure has
occurred as a result of maternal diet including fish and whale
meat, the strongest mercury effects were noted in motor and
attention performance (Debes et al. 2006) and persist into
adolescence. In addition, MeHg exposure can affect birth
weight, immune function (Lalancette et al. 2003; Das et al.
2008), and may, in some cases, be associated with organ
damage (Rawson et al. 1993). Damage that occurs during fetal
development may have lifelong effects, so the fetus is a cohort
of particular concern as are pregnant females (Davidson et al.
2006; Debes et al. 2006).
It is difficult to assess the effects of MeHg in wildlife
(Fig. 4). The toxic threshold for hair [THg] in terrestrial
mammals has been reported as 20 lg/g (Thompson 1996),
although there is a growing body of evidence linking chronic
MeHg exposure to more subtle effects including disruption of
brain neurochemistry (Basu et al. 2009). Dietz et al. (2011b)
have suggested that hair [THg] as low as 6 lg/g results in
subclinical alterations in brain biochemistry in polar bears.
According to the World Health Organization (WHO 1990)
human maternal hair concentrations of 10–20 lg/g may
Mercury Concentrations in Steller Sea Lion Hair 273
indicate exposure great enough to impact fetal neurodevel-
opment. The Agency for Toxic Substances and Disease Reg-
istry (ATSDR) determined that there were no adverse health
effects to the fetus associated with maternal hair [THg] under
15.3 lg/g (Risher and DeWoskin 1999). The Alaska Hair
Mercury Biomonitoring Program (AHMBP; State of Alaska
Epidemiology Bulletin 2010) targets women of childbearing
age with hair [THg] > 5 lg/g for follow-up assessment.
Similar thresholds have not been reported directly for fetal hair
[THg]; however, more than half the young pups from the
western DPS exceeded at least one of these thresholds and
three individuals exceeded them all. Two of these three indi-
viduals were also underweight for their age (*33 kg com-
pared to 48 ± 8 kg for the rest of the group). Brookens et al.
(2008) also noted low mass as well as clinical abnormalities in a
harbor seal pup with hair [THg] > 20 lg/g. We do not have
data from adult pregnant SSLs (another cohort of concern) in
this study but results from northern fur seals at St. Paul Island
in the Bering Sea of Alaska (Beckmen et al. 2002) suggest that
the values for hair [THg] in SSL dams would be higher than
those observed in their newborn pups.
In humans, hair [THg] is on average 250 times greater
than that of whole blood (Budtz-Jørgensen et al. 2004).
Most other mammals have a greater relative amount of hair
in which to distribute mercury, so the relationships be-
tween hair and whole blood concentrations are different.
Fish-fed Alaskan sled dogs have been shown to have 60-fold
higher [THg] in hair than blood (Lieske et al. 2011), while
in harbor seals a linear relationship has been observed with
hair concentrations only 22 (females) to 40 (males) times
higher than blood (Brookens et al. 2007). Applying human
hair thresholds to SSLs may be misleading as blood con-
centrations associated with hair [THg] in SSLs may be
higher than what one would observe in humans. Mea-
surements in harbor seal pups indicate that the pelt and
muscle contain the majority of total body burden of mer-
cury; the first by virtue of its high [THg] and the second by
virtue of its large contribution to total body mass (Broo-
kens et al. 2008). More information about mercury parti-
tioning in SSLs would be valuable.
Data from the AHMBP indicate that while [THg] in
hair from women of childbearing age is generally low in
Alaska (median values in different regions 0.29–0.78 lg/g),
concentrations from coastal regions are highest in the
southwest (includes AI), intermediate along the Gulf Coast
(includes CGOA and PWS), and lowest in the southeast
(includes SEA) (State of Alaska Epidemiology Bulletin
2010). Similar results from this study, including interme-
274 J. Margaret Castellini et al.
diate to high values throughout the western DPS and low
values in the eastern DPS, demonstrate the important
relationships between marine wildlife and coastal Alaskan
populations. All AHMBP participants with hair
[THg] > 5 lg/g were from the southwest coastal region,
and at least one was pregnant. As subsistence users, the
women regularly consumed marine mammal livers and
kidneys and/or large northern pike. The AHMBP is just a
snapshot into the health of coastal communities and indi-
cates a need to be aware of mercury in the marine envi-
ronment, including regional and temporal differences that
might exist.
Effects of toxicants can be mediated by the presence of
other contaminants, interaction with nutrients, nutritional
status, genetic predisposition, or development (Rice 2008).
The same marine diet that contains high levels of MeHg is
also typically rich in omega-3 fatty acids and selenium
which may provide some level of protection from the
toxicological effects of MeHg (Davidson et al. 2008). The
effects of MeHg on neurodevelopment may be augmented
by the presence of other environmental toxicants, partic-
ularly PCBs (Roegge et al. 2004; Rice 2008). There may also
be genetically mediated differences in the physiological and
biochemical response to MeHg exposure (Custodio et al.
2004; Gundacker et al. 2007). The western and eastern
DPSs of SSLs are genetically distinct (Bickham et al. 1996)
and may be a separate subspecies (Phillips et al. 2009),
which might also contribute to the [THg] differences ob-
served between the pups from the two DPSs.
Biomarkers are an important link for relating con-
taminant exposure to health. An array of biomarkers
measured in concert, including biomarkers of exposure,
susceptibility, and effect, is key to gaining a complete
understanding of risk factors (Ryan et al. 2007) and, in the
case of marine mammals, potential adaptive mechanisms
associated with piscivory. The use of such an approach is
chemical specific. Some biomarkers that might be effective
in assessing effects, risk factors, and adaptive population
differences associated with mercury exposure include
metallothionein expression, glutathione peroxidase activity,
and selenium concentrations (Gundacker et al. 2007;
Woshner et al. 2008). Levels of muscarinic cholinergic
receptors and N-methyl-D-aspartate (NMDA) glutamate
receptors are among a suite of potential neurochemical
biomarkers in brain (Basu et al. 2009). Stable isotope
analysis is valuable for assessing potential dietary compo-
nents of exposure. Methylmercury binds preferentially to
sulfur moieties within proteins and is strongly associated
with hair and red blood cells (Airey 1983; Woshner et al.
2008). Marine mammals tend to have elevated blood vol-
umes, hemoglobin, and myoglobin content (Lenfant et al.
1970; Castellini and Somero 1981; Castellini et al. 1996)
which might play an important adaptive role in how MeHg
is partitioned among tissues and its bioavailability. In the
case of the SSL pups in this study, hair may be an efficient
excretory route for MeHg during fetal development when
vulnerability to exposure is high. This partitioning of
mercury into hair may prove to be highly adaptive in
marine mammals in general and a good method for
assessing mercury exposure in the critical cohort of an
ecosystem’s mammalian piscivores.
CONCLUSION
Methylmercury is eliminated by the hair making it a useful
biomonitoring tool for assessing ecosystem health. In this
study, we used archived hair samples to assess mercury
exposure in Alaskan SSLs with greater resolution, both
temporally and regionally than has been done previously.
As apex marine predators, SSLs are an important sentinel
species in Alaska and have undergone drastic population
changes as a result of a changing environment. Based on
data from hair, the regions containing the endangered
western DPS have a higher mercury exposure, though
exposure levels were not directly correlated to trends in pup
production during the study period. These regions overlap
those with the greatest human exposure (State of Alaska
Epidemiology Bulletin 2010), emphasizing the value of
SSLs as marine sentinels. Because pups within this DPS are
exposed in utero, the consequences of fetal exposure are of
concern in this population. Methylmercury exposure can
affect birth weight as well as neurological and immuno-
logical development, potentially affecting recruitment. In
this study, many of the pups exposed in utero exceeded
biomonitoring thresholds established for human maternal
hair and other wildlife. As SSL dams might have higher
[THg] than their pups and marine mammal hair [THg]
could indicate higher corresponding blood [THg] than in
humans, these results indicate a need for increased atten-
tion to the role of MeHg exposure to SSL health. Body
burden and partitioning (toxicodistribution) studies and
identification of biomarkers to assess effects, risk, and
population differences are keys to understanding the
implications of MeHg exposure and potential adaptive re-
sponses associated with piscivory. The effects of environ-

mental change on future mercury deposition, bioavail-
ability, and biomagnifications are not clear. Continued
biomonitoring of sentinel species such as SSLs will provide
valuable insights into changing ecosystem health.
ACKNOWLEDGMENTS
We thank the field research teams of both the Alaska
Department of Fish and Game and the National Marine
Mammal Laboratory (NMFS/NOAA), the staff of the Alaska
SeaLife Center (ASLC), and the crews of the R/V Medeia, P/V
Stimson, P/V Wolstad, R/V Tiglax, M/V Pacific Star, and the
R/V Norseman. We thank Darce Holcomb of the Wildlife
Toxicology Laboratory, University of Alaska Fairbanks, for
assistance with sample analysis and Tom Gelatt of the National
Marine Mammal Laboratory for providing manuscript com-
ments. Funding has been provided through NOAA Cooper-
ative Agreements NA17FX1079, NA04NMF4390170, and
NA07NMF4390312. In addition, this publication was made
possible by Grant Number 5P20RR016466 from the National
Center for Research Resources (NCRR), a component of the
National Institutes of Health (NIH). Sample collection
described here was part of ongoing Steller sea lion research
conducted by the Alaska Department of Fish and Game, The
National Marine Mammal Laboratory and the Alaska SeaLife
Center under MMPA permits #358-1564, 358-1769, 358-1888,
782-1889, and 881-18900-02 and under ADFG ACUC #03-
002 and #06-07 and ASLC IACUC Protocol 07-001.
REFERENCES
Aguirre AA, Tabor GM (2004) Introduction: marine vertebrates as
sentinels of marine ecosystem health. EcoHealth 1:236–238
Airey D (1983) Mercury in human hair due to environment and
diet: a review. Environmental Health Perspectives 52:303–316
Anderson PJ, Piatt JF (1999) Community reorganization in the
Gulf of Alaska following ocean climate regime shift. Marine
Ecology Progress Series 189:117–123
Ashwell-Erickson S, Fay FH, Elsner R, Wartzok D (1986)
Metabolic and hormonal correlates of molting and regenera-
tion of pelage in Alaskan harbor and spotted seals (Phoca
vitulina and Phoca largha). Canadian Journal of Zoology 64:
1086–1094
Basu N, Scheuhammer AM, Sonne C, Letcher RJ, Born EW, Dietz
R (2009) Is dietary mercury of neurotoxicological concern to
wild polar bears (Ursus maritimus)? Environmental Toxicology
and Chemistry 28:133–140
Beckmen KB, Duffy LK, Zhang X, Pitcher KW (2002) Mercury
concentrations in the fur of Steller sea lions and northern fur
seals from Alaska. Marine Pollution Bulletin 44:1130–1135
Mercury Concentrations in Steller Sea Lion Hair 275
Bemis JC, Seegal RF (1999) Polychlorinated biphenyls and
methylmercury act synergistically to reduce rat brain dopamine
content in vitro. Environmental Health Perspectives 107:879–885
Bickham JW, Patton JC, Loughlin TR (1996) High variability for
control region sequences in a marine mammal: implications for
conservation and biogeography of Steller sea lions. Journal of
Mammalogy 77:95–108
Bossart GD (2006) Marine mammals as sentinel species for oceans
and human health. Oceanography 19(2):134–137
Brookens TJ, Harvey JT, O’Hara T (2007) Trace element con-
centrations in the Pacific harbor seal (Phoca vitulina richardii)
in central and northern California. Science of the Total Envi-
ronment 372:676–692
Brookens TJ, O’Hara TM, Taylor RT, Bratton GR, Harvey JT
(2008) Total mercury body burden in Pacific harbor seal, Phoca
vitulina richardii, pups from central California. Marine Pollution
Bulletin 56:27–41
Budtz-Jørgensen E, Grandjean P, Jørgensen PJ, Weihe P, Keiding
N (2004) Association between mercury concentrations in blood
and hair in methylmercury-exposed subjects at different ages.
Environmental Research 95:385–393
Burbacher TM, Rodier PM, Weiss B (1990) Methylmercury and
developmental neurotoxicity: a comparison of effects in humans
and animals. Neurotoxicology and Teratology 12:191–202
Burek KA, Gulland FMD, Sheffield G, Beckmen KB, Keyes E,
Spraker T, et al. (2005) Infectious disease and the decline of
Steller sea lions (Eumetopias jubatus) in Alaska, USA: insights
from serological data. Journal of Wildlife Diseases 41:512–524
Castellini MA, Somero GN (1981) Buffering capacity of vertebrate
muscle: correlations with potential for anaerobic function.
Journal of Comparative Physiology 143:191–198
Castellini JM, Meiselman HJ, Castellini MA (1996) Understanding
and interpreting hematocrit measurements in pinnipeds. Mar-
ine Mammal Science 12:251–264
Castoldi AF, Coccini T, Ceccatelli S, Manzo L (2001) Neurotox-
icity and molecular effects of methylmercury. Brain Research
Bulletin 55(2):197–203
Clarkson TW (1994) The toxicology of mercury and its com-
pounds. In: Mercury Pollution: Integration and Synthesis, Watras
CJ, Hackabee JW (editors), Boca Raton, FL: CRC Press, pp 631–
642
Custodio HM, Broberg K, Wennberg M, Jansson J-H, Vessby B,
Hallmans G, et al. (2004) Polymorphisms in glutathione-related
genes affect methylmercury retention. Archives of Environmental
Health 59:588–595
Das K, Siebert U, Gillet A, Dupont A, Di-Poı̈ C, Fonfara S, et al.
(2008) Mercury immune toxicity in harbor seals: links to in
vitro toxicity. Environmental Health 7:52–68
Davidson PW, Myers GJ, Cox C, Wilding GE, Shamlaye CF,
Huang LS, et al. (2006) Methylmercury and neurodevelopment:
longitudinal analysis of the Seychelles child development co-
hort. Neurotoxicology and Teratology 28:529–535
Davidson PW, Strain JJ, Myers GJ, Thurston SW, Bonham MP,
Shamlaye CF, et al. (2008) Neurodevelopmental effects
of maternal nutritional status and exposure to methylmercury
from eating fish during pregnancy. NeuroToxicology 29:767–
775
Debes F, Budtz-Jørgensen E, Weihe P, White RF, Grandjean P
(2006) Impact of prenatal methylmercury on neurobehavioral
function at age 14 years. Neurotoxicology and Teratology 28:536–
547
276 J. Margaret Castellini et al.
DeMaster DP, Trites AW, Clapham P, Mizroch S, Wade P, Small
RJ, et al. (2006) The sequential megafaunal collapse hypothesis:
testing with existing data. Progress in Oceanography 68:329–342
Dietz R, Basu N, Braune B, O’Hara T, Scheuhammer T, Sonne C
(2011a) What are the toxicological effects of mercury in arctic
biota? In: AMAP Assessment 2011: Mercury in the Arctic,
Outridge P, Dietz R, Wilson S (editors), Oslo, Norway: Arctic
Monitoring and Assessment Programme (AMAP), pp 113–137.
Dietz R, Born EW, Rigét F, Aubail A, Sonne C, Drimmie R, et al.
(2011) Temporal trends and future predictions of mercury
concentrations in northwest Greenland polar bear (Ursus
maritimus) hair. Environmental Science and Technology 45:1458–
1465
Fritz L, Gelatt T (2010) Surveys of Steller sea lions in Alaska, June–
July 2010. In: Memorandum to the Record, National Marine
Mammal Laboratory, National Marine Fisheries Service 7600
Sand Point Way NE, Seattle, WA 98115 31 pp. http://www.afsc.
noaa.gov/nmml/PDF/SSL-Survey-memo-2010.pdf. Accessed Jan
3, 2011.
Gulland F (1999) Stranded seals: important sentinels. Journal of
the American Veterinarian Medical Association 214(8):1191–
1192
Grandjean P, Weihe P, White RF, Debes F, Araki S, Yokoyama K,
et al. (1997) Cognitive deficit in 7-year-old children with pre-
natal exposure to methylmercury. Neurotoxicology and Teratol-
ogy 19:417–428
Gundacker C, Komarnicki G, Jagiello P, Gencikova A, Dahmen N,
Wittmann KJ, et al. (2007) Glutathione-S-transferase poly-
morphism, metallothionein expression, and mercury levels
among students in Austria. Science of the Total Environment
385:37–47
Holmes AL, Wise SS, Goertz CEC, Dunn JL, Gulland FMD, Gelatt
T, et al. (2008) Metal tissue levels in Steller sea lion (Eumetopias
jubatus) pups. Marine Pollution Bulletin 56:1416–1421
Jones D, Ronald K, Lavigne DM, Frank R, Holdrinet M, Uthe JF
(1976) Organochlorine and mercury residues in the harp seal
(Pagophilus groenlandicus). Science of the Total Environment
5:181–195
King JC, Gelatt TS, Pitcher KW, Pendelton GW (2007) A field-
based method for estimating age in free-ranging Steller sea lions
(Eumetopias jubatus) less than twenty-four months of age.
Marine Mammal Science 23(2):262–271
Kirk CM, Amstrup S, Swor R, Holcomb D, O’Hara TM (2010)
Hematology of Southern Beaufort Sea polar bears (2005–2007):
biomarker for an arctic ecosystem health sentinel. EcoHealth
7(3):307–320
Kirk CM, Amstrup S, Swor R, Holcomb D, O’Hara TM (2010)
Morbillivirus and Toxoplasma exposure and association with
hematological parameters for Southern Beaufort Sea polar
bears: potential response to infectious agents in a sentinel spe-
cies. EcoHealth 7(3):321–331
Knott KK, Schenk P, Beyerlein S, Boyd D, Ylitalo GM, O’Hara TM
(2011) Blood-based biomarkers of selenium and thyroid status
indicate possible adverse biological effects of mercury and bi-
chlorinated biphenyls in Southern Beaufort Sea polar bears.
Environmental Research 111:1124–1136
Lalancette A, Morin Y, Measures L, Fournier M (2003) Con-
trasting changes of sensitivity by lymphocytes and neutrophils
to mercury in developing grey seals. Developmental and Com-
parative Immunology 27:735–747
Lieske CL, Moses SK, Castellini JM, Klejka J, Hueffer K, O’Hara
TM (2011) Toxicokinetics of mercury in blood compartments
and hair of fish-fed sled dogs. Acta Veterinaria Scandinavica
53:66. doi:10.1186/175-0147-53-66. Online Dec 7, 2011.
Lenfant C, Johansen K, Torrance JD (1970) Gas transport and
oxygen storage capacity in some pinnipeds and the sea otter.
Respiratory Physiology 9:277–286
Loughlin TR (1998) The Steller sea lion: a declining species. Bi-
oshphere Conservation 1:91–98
Loughlin TR, Perlov AS, Vladimirov VA (1992) Range-wide sur-
vey and estimation of total number of Steller sea lions in 1989.
Marine Mammal Science 8:220–239
Mathews EA, Womble JN, Pendleton GW, Jemison LA, Manisc-
alco JM, Streveler G (2011) Population growth and colonization
of Steller sea lions in the Glacier Bay region of southeastern
Alaska: 1970s–2009. Marine Mammal Science 27(4):852–880
Merrick RL (1997) Current and historical roles of apex predators
in the Bering Sea ecosystem. Journal of Northwest Atlantic
Fishery Science 22:343–355
Merrick RL, Loughlin TR, Calkins DG (1987) Decline in abun-
dance of the northern sea lion (Eumetopias jubatus) in Alaska,
1956–86. Fisheries Bulletin 85:351–365
National Research Council (1996) The Bering Sea Ecosystem,
Washington, DC: The National Academies Press, pp 308
National Marine Fisheries Service (1997) Threatened fish and
wildlife: change in listing status of Steller sea lions under the
endangered species act. Federal Register 62:24345–24355
National Marine Fisheries Service (2008) Recovery plan for the
Steller sea lion (Eumetopias jubatus). Revision. National Marine
Fisheries Service, Silver Spring, MD. 325 pp.
Oken E, Wright RO, Kelinman KP, Bellinger D, Amarasirwardena
CJ, Hu H, et al. (2005) Maternal fish consumption, hair mer-
cury, and infant cognition in a US cohort. Environmental Health
Perspectives 113(10):1376–1380
Oskarsson A, Palminger HI, Sundberg J (1995) Exposure to toxic
elements via breast milk. Analyst 120(3):765–770
Oskarsson A, Palminger HI, Sundberg J, Petersson Grawé K
(1998) Risk assessment in relation to neonatal metal exposure.
Analyst 123(1):19–23
Phillips CD, Bickham JW, Patton JC, Gelatt TS (2009) Systematics
of Steller sea lions (Eumetopias jubatus): subspecies recognition
based on concordance of genetics and morphometrics. Occa-
sional Papers, Museum of Texas Tech University 283:1–15.
Pitcher KW, Burkanov VN, Calkins DG, Le Boeuf BJ, Mamaev
EG, Merrick RL, et al. (2001) Spatial and temporal variation in
the timing of births of Steller sea lions. Journal of Mammalogy
82(4):1047–1053
Rawson AJ, Patton GW, Hofmann S, Pietra GG, Johns L (1993)
Liver abnormalities associated with chronic mercury accumu-
lation in stranded Atlantic bottlenose dolphins. Ecotoxicology
and Environmental Safety 25:41–47
Rea LD, Banks AR, Farley SD, Stricker CA, Fadely BS, Pitcher
KW (2011) Regional differences in age of weaning in Steller
sea lions determined using stable isotopes of carbon and
nitrogen. Alaska Marine Science Symposium, Jan 17–20, 2011,
Anchorage, Alaska.
Reddy ML, Dierauf LA, Gulland FMD (2001) Marine mammals as
sentinels of ocean health. In: CRC Handbook of Marine Mammal
Medicine, Dierauf LA, Gulland FMD (editors), Boca Raton, FL:
CRC Press, pp 3–14
Rice DC (2008) Overview of modifiers of methylmercury neuro-
toxicity: chemicals, nutrients, and the social environment.
Neurotoxicology 29:761–766

Risher J, DeWoskin R (1999) Health effects: relevance to public
health In: Toxicological Profile for Mercury, Atlanta, GA: US
Department of Health and Human Services, Public Health
Service, Agency for Toxic Substances and Disease Registry
(ATSDR), pp 220–300. http://www.atsdr.cdc.gov/toxprofiles/
tp46.pdf. Accessed Dec 29, 2011.
Roegge CS, Wang VC, Powers BE, Klintsova AY, Villareal S,
Greenough WT, et al. (2004) Motor impairment in rats exposed
to PCBs and methylmercury during early development. Toxi-
cological Sciences 77:315–324
Ryan PB, Burke TA, Cohen Hubal EA, Cura JJ, McKone TE
(2007) Using biomarkers to inform cumulative risk assessment.
Environmental Health Perspectives 115(5):833–840
Sinclair EH, Zeppelin TK (2002) Seasonal and spatial differences
in diet in the western stock of Steller sea lions (Eumetopias
jubatus). Journal of Mammalogy 83:973–990
Springer AM, Estes JA, van Vliet GB, Williams TM, Doak DF,
Danner EM, et al. (2003) Sequential megafaunal collapse in the
North Pacific Ocean: an ongoing legacy of industrial whaling?
Proceedings of the National Academy of Sciences of the United
States of America 100:12223–12228
State of Alaska Epidemiology Bulletin (2010) Alaska hair bio-
monitoring program update, July 2002–May 2010. Division of
Health, Department of Health and Social Services. 3601 C
Street, Ste 540, Anchorage, AK, 99503. Bulletin 18, June
24, 2010. http://www.epi.hss.state.ak.us/bulletins/docs/b2010_
18.pdf. Accessed Dec 29, 2011.
Thompson DR (1996) Mercury in birds and terrestrial mammals.
In: Environmental Contaminants in Wildlife. Interpreting Tissue
Concentrations. Nelson Beyer W, Heinz GH, Redmon-Norwood
Mercury Concentrations in Steller Sea Lion Hair 277
AW (editors) SETAC Special Publications Series, New York:
CRC Press, pp 341–356.
Trites AW, Donnelly CP (2003) The decline of Steller sea lions in
Alaska: a review of the nutritional stress hypothesis. Mammal
Review 33:3–28
Trites AW, Livingston PA, Mackinson S, Vasconcellos C, Springer
AM, Pauly D (1999) Ecosystem change and the decline of
marine mammals in the eastern Bering Sea: testing the ecosys-
tem shift and commercial whaling hypotheses. Fisheries Centre
Research Reports 7, Vancouver, British Columbia, Canada: The
Fisheries Centre, University of British Columbia. 106 pp.
Wagemann R, Stewart REA, Lockhart WL, Stewart BE, Provoledo
M (1988) Trace metals and methyl mercury: associations and
transfer in harp seal (Phoca groenlandica) mothers and their
pups. Marine Mammal Science 4:339–355
Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM
(2003) Ecotoxicology of mercury. In: Handbook of Ecotoxicology,
Hoffman DJ, Rattner BA, Burton GA Jr, Cairns J Jr (editors),
2nd ed. Boca Raton, FL: Lewis Publishers, pp 409–464
World Health Organization (1990) Environmental health criteria for
methylmercury: Evaluation of human health risks. In: Environ-
mental Health Criteria 101, Geneva, Switzerland: International
Programme on Chemical Safety (IPCS). http://www.inchem.
org/documents/ehc/ehc/ehc101.htm. Accessed Dec 29, 2011.
Woshner V, Knott K, Wells R, Willetto C, Swor R, O’Hara T
(2008) Mercury and selenium in blood and epidermis of bot-
tlenose dolphins (Tursiops truncates) from Sarasota Bay, FL:
interaction and relevance to life history and hematological
parameters. EcoHealth 5:360–370