Mercury concentrations in the fur of Steller sea lions andnorthern fur seals from Alaska

Kimberlee B. Beckmen a,*, Lawrence K. Duffy b, Xiaoming Zhang b, Kenneth W. Pitcher c

a Department of Veterinary Biosciences, College of Veterinary Medicine, University of Illinois at Urbana-Champaign,

2001 S. Lincoln Avenue, Urbana, IL 61802, USAb Department of Chemistry and Biochemistry, University of Alaska Fairbanks, Fairbanks, AK 99775, USA

c Alaska Department of Fish and Game, Division of Wildlife Conservation, 333 Raspberry Road, Anchorage, AK 99518, USA

Abstract

We compared total mercury (THg) concentrations in the fur of northern fur seals (Callorhinus ursinus) from the depleted Pribilof

Islands population with those of both declining and thriving populations of Steller sea lions (Eumetopias jubatus) from Prince

William Sound (PWS) and Southeast Alaska (SEA), respectively. Relatively low wet weight concentrations (ranges) of THg were

detected in the fur of Steller sea lion (SSL) pups (0.90–3.14 lg/g) and juveniles (0.56–6.75 lg/g) from both areas in 1998 and 2000

compared to northern fur seal (NFS) pups (3.15–8.14 lg/g) in 2000. The mean concentration � SD for SSLs sampled were

1:46� 0:64 lg/g for pups (n ¼ 22) and 2:74� 2:89 lg/g for juveniles (n ¼ 6). Analyses indicated higher THg concentrations from

SSL pups from PWS compared to the SEA. Mean � SD. THg in the NFS pups was 4:90� 1:42 lg/g (n ¼ 34) and for post-partum

dams was 7:84� 1:78 lg/g (n ¼ 12).

� 2002 Elsevier Science Ltd. All rights reserved.

Keywords: Mercury; Marine mammals; Steller sea lions; Northern fur seals; Alaska

1. Introduction

Pinnipeds, because of their position in the food webas high trophic level predators, are key indicators of

change in the environment. Several populations of

pinnipeds in Alaska have experienced unexplained de-

clines in recent decades. For example, during the sum-

mer breeding season, 74% of the world’s population of

northern fur seals (Callorhinus ursinus) are on the Pri-

bilof Islands and the numbers of pups born declined at

a rate of 6.5–7.8% per year in the 1980s, and the declinehas continued thereafter on St. George Island (York,

1987; York et al., 1998). Currently the entire stock

is listed as ‘‘depleted’’ under the Marine Mammal

Protection Act. Although the proximate causes for

this decline are unknown, some potential risk factors

are under investigation (Beckmen, 1999). Moreover, a

sympatric otariid species, the Steller sea lion (Eumet-

opias jubatus) has declined markedly in the last 30 years,

with a loss of over 80% of the population from the

western stock (Merrick et al., 1987; Loughlin et al.,1992; Sease et al., 2001). The genetically distinct eastern

stock of Steller sea lions (SSLs) in Southeastern Alaska

on the other hand, has nearly doubled during the same

time period (Calkins et al., 1999). The causes of the

precipitous decline in numbers are undetermined and

resulted in a classification of ‘‘endangered’’ for the

western stock (west of 144�W) under the U.S. Endan-

gered Species Act in 1997 while the eastern stock re-mained classified as ‘‘threatened’’.

Researchers have suggested that the early decline of

SSL in the 1970s could have been due to nutritional

stress resulting in reduced survivorship (Merrick, 1995;

Calkins et al., 1998) and reduced fecundity (Pitcher et al.,

1998). However, there is no solid evidence linking

undernutrition to the recent population decline (Calkins

et al., 1998) and multiple factors operating on the pop-ulation temporally and spatially have been suggested

(DeMaster et al., 2001). At this time, chemical pollu-

tants cannot be ruled out. Environmental contaminants

have been mentioned as a possible factor in the recent

*Corresponding author. Tel.: +1-217-333-9362; fax: +1-217-244-

1652.

E-mail address: beckmen@uiuc.edu (K.B. Beckmen).

0025-326X/02/$ - see front matter � 2002 Elsevier Science Ltd. All rights reserved.

PII: S0025-326X(02 )00167 -4

www.elsevier.com/locate/marpolbul

Marine Pollution Bulletin 44 (2002) 1130–1135

decline of SSL (Merrick et al., 1995; Merrick, 1995) buttheir potential importance has not been evaluated. Re-

ports of contaminant concentrations for SSL are sparse.

Only a single report of mercury concentrations was

found in the published literature and it pertained to

sampling in California, which is at the extreme southern

end of the range of the eastern stock (Sydeman and

Jarman, 1998).

Here, we report and compare total mercury (THg)concentrations in fur from northern fur seal (NFS) pups

and dams, and SSL pups and juveniles from two stocks.

2. Methods

Twenty eight and thirty nine fur samples were col-

lected from SSL and NFS, respectively, during livecapture/release studies conducted during 1998 and 2000.

The SSL were live captured near haulout sites in Alas-

kan coastal waters in Southeastern Alaska (SEA; Ben-

jamin Island 58�560N, 134�910W) during November

1998 and January 2000, and at four haulout sites in

Prince William Sound (PWS; 60�070N 147�370W) during

April 2000 (Fig. 1). The NFS were captured on breeding

rookeries on St. Paul Island (57�110N 170�290W) duringJuly and August 2000 (Fig. 1). Animals were captured

and handled under Marine Mammal Protection Act

permits 758-1459-01, 965, 782-1455, 675-1, and 358-

1564-00 issued by the Office of Protected Resources of

the National Marine Fisheries Service.

NFSs were sampled opportunistically from the top of

head where an identifying mark was made by clipping

the fur as well as from sites on the dorsum of the neck(pups) or flank (adult females) that were prepared for

other procedures. The majority of the NFS captures

were directed at pups but when a dam and pup were

captured as a pair, the dam was also sampled. All SSL

fur samples were collected from the flank area where a

site was prepared for other procedures.

Both NFS and SSL are otarid pinnipeds that retain

their lanugo natal coat after birth and molt later duringthe nursing period. All NFS pups were sampled before

molting of the natal coat; two cases were stillborn fe-tuses. SSLs under one year of age were considered pups

and those older, juveniles. At sampling, SSL pelage was

evaluated and classified as natal coat, post-natal molt,

or juvenile coat. Samples consisted mainly of guard

hairs but underfur was also collected. Samples were re-

moved with scissors, placed directly in Whirlpac� bags,

and stored cold until analyzed. Prior to sample prepa-

ration, each sample was washed with a mild detergentand rinsed with water. THg was analyzed at Fron-

tier Geosciences (Seattle, WA) by cold vapor atomic

fluorescence spectrophotometry (CVAF) after digestion

with acid (Bloom, 1992; Bloom and Fitzgerald, 1998).

For THg, the sample was transferred to a pre-cleaned

vial, to which 70% HNO3/30% H2SO4 was added. The

samples were heated on a hotplate at 90 �C until dis-

solved. After cooling, the digests were diluted with 10%0.2 N BrC1. Aliquots of digests were reduced with

SnC12 concentrated by gold amalgamation, followed by

CVAF detection (EPA method 1631). The mean detec-

tion limit (MDL) for THg was 0.5 ng/g and results are

reported on a wet weight basis. To assess recoveries and

accuracy certified dogfish tissue reference material

(DORM-2) was analyzed. The average recovery for THg

was 88% (range 85–90%) for the published values forDORM-2. Analytical differences between duplicates

averaged 5% ranging from 0.4% to 6.1%. Percent re-

coveries based on analytical spikes averaged 98%, and

ranged from 93.9% to 103%.

Statistical analyses were carried out using Sigma Stat

2.03 software (SPSS Inc., Chicago, IL). Concentrations

were compared using one way ANOVA with Tukey’s

tests. A level of a ¼ 0:05 was chosen to detect differ-ences.

3. Results

3.1. Mercury in fur of Steller sea lions

The mercury concentrations in fur of SSLs collected

in 1998 and 2000 are listed in Table 1. There was no

significant difference detected between the THg con-

centrations in fur from male and female pups. The THg

concentration for the only juvenile male SSL fur samplecollected was at the low end of the range for similarly

aged females. When results from both sexes were com-

bined by age and capture location, juvenile SSLs in PWS

had significantly higher THg compared to juveniles in

SEA (4.89 vs. 0.59 lg/g w.w. (wet weight); p ¼ 0:048,n ¼ 3 each area with juvenile winter pelage) (Fig. 2).

SSL pups from PWS also had significantly higher THg

in fur than pups from SEA (1.68 vs. 1.14 lg/g w.w.,p ¼ 0:046, n ¼ 13 and 9) but PWS pups had generally

undergone a post-natal molt prior to sampling while

SEA pups were still in natal fur (Fig. 2).Fig. 1. Capture sites of NFSs and SSLs sampled in 1998 and 2000.

K.B. Beckmen et al. / Marine Pollution Bulletin 44 (2002) 1130–1135 1131

3.2. Mercury in fur of NFSs

Concentrations of THg in fur of NFS pups and post-

partum dams collected in 2000 are listed in Table 2.

There was no significant difference between male and

female NFS pups (all in natal coat). The mean THgconcentration for all NFS pups was 4:90� 1:42 lg/gw.w. (n ¼ 34). There was no significant correlation be-

tween THg concentrations in fur of the NFS dams and

their pups (Table 1; Fig. 3). In general, the pups had

lower THg than their own dams. However, of the 12

pairs sampled, all the dams had higher THg than their

respective pups, except for 2, and one of these was the

oldest dam sampled. The THg concentrations in fur ofthe post-parturient dams was significantly greater than

that of their pups (p ¼ 0:001) and the mean of all pups

sampled (p < 0:0001).

3.3. Comparison of mercury in fur between species

Juvenile SSL THg concentrations (2:74� 2:89 lg/gw.w., n ¼ 6; p ¼ 0:009) were significantly lower thanthose of the NFS pups (4:90� 1:42 lg/g w.w., n ¼ 34).

Additionally, all SSL pup THg concentrations were

below the range of the NFS pups (Tables 2 and 3).

4. Discussion

The northern fur seal THg values presented werehigher than those in fur from similarly aged animals

reported in the past (Table 3) (Kim et al., 1974). In most

previous studies, mercury concentrations in fur seals

were determined on liver, but liver samples were not

available in this non-invasive, opportunistic study

(Anas, 1974; Goldblatt and Anthony, 1983; Zeisler et al.,

1993). The high concentrations of mercury found in fur

seal liver in the 1970s prompted an investigation of

Table 1

Range, median, and mean� SD concentrations of total mercury in fur

(lg/g w.w.) of pup and juvenile SSLs from Southeast Alaska and

Prince William Sound (Gulf of Alaska), live-captured from 1998 to

2000

Range Median Mean SD n

Female pups

<12 months

0.90–3.05 1.35 1.41a �0.55 13

Male pups

<12 months

0.97–3.14 1.15 1.52a �0.76 9

Female juve-

niles 20–22

months

0.56–6.75 1.86 3.17 �3.01 5

Male juvenile

20 months

0.59 1

aNo significant difference between sexes.

Fig. 2. THg concentrations (lg/g wet weight) in fur from pup and

juvenile SSLs in Alaska in 1998 and 2000 by location and approximate

age in months.

Table 2

Range, median, and mean� SD concentrations of mercury in fur (lg/gw.w.) of pup and post-partum adult female NFSs from St. Paul Island

Alaska in 2000

Range Median Mean SD n

Female

pups <1

month

3.16–7.89 4.65 4.87b �1.34 26

Male pups

<1 month

3.15–8.14 4.85 5.03b �0.76 8

Adult

females

5.89–12.10 7.39 7.84 �1.78 12

bNo significant difference between sexes.

Fig. 3. THg concentrations (lg/g wet weight) in fur of 12 dam/pup

pairs collected on St. Paul Island, AK in 2000. Concentrations in pairs

were not significantly correlated (r2 ¼ 0:0257).

1132 K.B. Beckmen et al. / Marine Pollution Bulletin 44 (2002) 1130–1135

potential public health problems among the Aleut na-

tives who were consuming the animals, but no adverse

health effects on consumers were found. Mercury tends

to accumulate with age in fur seals so finding higher

concentrations in adults than pups was expected (Anas,

1973; Anas, 1974; Bacher, 1985; Noda et al., 1995). It is

perplexing that stillborn and newborn pup fur was not

positively correlated to their respective dams consider-ing mercury is transported transplacentally in other

pinnipeds (Wagemann et al., 1988).

Since mercury is bioaccumulated in predators, the

significantly higher mercury concentrations in the fur of

NFS pups in this study compared to older SSL pups and

juveniles are likely differences in prey selection by the

dam but may be due to geographic differences. Based on

scat analysis and stomach contents collected historically,prey species chosen by NFS and SSL overlap but NFS

females tend to eat more squid and less of certain fin fish

than SSLs (Pitcher, 1981; Perez and Bigg, 1986; An-

tonelis et al., 1997; Mori et al., 2001). Additionally, NFS

females migrate during winter to pelagic feeding areas in

the North Pacific Ocean but feed in the Bering Sea

during the summer. Pregnant and lactating SSL females

are not highly migratory and tend to feed closer torookeries or haulout sites in coastal areas. Thus, prey

species available in these areas will likely differ. The

stock differences detected in Hg concentrations among

SSL pups of different locations is more likely a function

of natal vs. post-natal molt but may also be attributed to

geographic differences or prey selection by SSLs in those

areas.

Despite the differences in age groups sampled be-tween stocks, which warrant caution in interpretation,

the overall result is that mercury concentrations are

relatively low in fur of subadult Alaskan SSL. In the

only published study documenting mercury concentra-

tions in SSLs (from California in 1993), Sydeman and

Jarman (1998) considered concentrations in liver to be

‘‘high’’ and the authors suggested both mercury and

copper be studied further as potential factors in the ir-

regular reproductive activities and population decline of

the species in California. However, the concentrations of

THg in SSL liver were lower (range 4.8–73.0, mean 19.0

lg/g d.w. (dry weight)) than for northern fur seal liver in

1992 (range 3.03–61.2, mean 26.7, SD 18.1 lg/g w.w.)

(Noda et al., 1995; Sydeman and Jarman, 1998). Of

note, this interspecies relationship with THg in liver

parallels that noted with the fur samples in this study.While mercury concentrations appear low in SSL fur,

similar to concerns for human, scientists must monitor

for the effect these that low level Hg exposure may have

on fetal development and juvenile or adult behavior.

There is a general understanding that methylmercury

(MeHg) is a significant neurotoxicant and that, with

chronic exposure at low concentrations, subtle effects

occur. The level of exposure to MeHg associated witheffects on the developing brain and immune systems

remain to be adequately characterized in marine mam-

mals. Low level exposure of Alaskan pinnipeds to MeHg

should be expected based on recent data in MeHg in

salmon (Zhang et al., 2001). The Hg in salmon muscle

was 62 ng/g, and muscle from a Steller sea lion collected

in the Aleutians had a THg of 1650 ng/g (Duffy, un-

published data).Potential interactive effects among mercury and other

contaminants at comparatively low levels also warrant

concern in the pinniped species we studied. Studies on

the developmental neurotoxicity of MeHg in humans

and laboratory animals have shown neurological and

neuropsychological effects, and laboratory animal stud-

ies have suggested that MeHg is more toxic in the

presence of polychlorinated biphenyls (PCBs) (Burb-acher et al., 1990; Weihe et al., 1998; Bemis and Seegal,

1999). Residues of PCBs in a subset of the present co-

hort of NFS and SSL and their immune function and

health status are under study and the results will be re-

ported elsewhere. Thus, synergism of multiple contam-

inant exposure in the neonate may be a mechanism of

adverse impact on the health of either NFS or SSL at

the concentrations measured in this study.

Table 3

Mean, range, and SD concentrations of THg (in lg/g w.w. or d.w.) in fur of two species of fur seals and two species of sea lions from the literature

Common name Species Year Mean SD or range n Notes

NFS C. ursinus 1972a 3.68 2 newborns

NFS C. ursinus 1972a 5.36 2 2 month-old pups

NFS C. ursinus 1972a 4.87 2 post-partum

females

Australian fur seal Arctocephalus

pusillus

1980sb 9.59 (d.w.) �5.89 16 6–144 months of

age

California sea lion Zalophus califor-

nianus

1970c 15.60 11.5–19.7 2

Southern sea lion Otaria flavescens 1995d 19.16 (d.w.) �12.87 7

aKim et al. (1974).b Bacher (1985).c Buhler and Mate (1973).d Fossi et al. (1997).

K.B. Beckmen et al. / Marine Pollution Bulletin 44 (2002) 1130–1135 1133

Although mercury cannot be linked directly to thedeclines of these populations, the differences between

body burdens in the endangered (higher concentrations)

and thriving (lower concentrations) stocks of the

SSL warrant further investigation of potential health

impact and continued monitoring. Additionally, since

Aleut natives consume these species as a part of the

traditional subsistence diet in the Aleutians and on the

Pribilof Islands, monitoring of mercury concentrationsshould continue to accommodate human health con-

cerns.

Acknowledgements

This research was funded in part by the North Pacific

Marine Research Program at the University of AlaskaFairbanks (UAF), the Cooperative Institute for Arctic

Research, and National Institute of Environmental

Health Sciences pilot grant from the University of

Washington’s Center for Ecogenetics, and the UAF

Water and Environmental Research Center through the

U.S. Geological Survey State Water Research Institute

Program. We gratefully acknowledge the additional

contributions of K. Burek, J. Mellish, B. Robson, L.Levin, S. Harper, and the many Alaska Department of

Fish and Game as well as the National Marine Mam-

mal Laboratory capture crew members assisted in the

collection of samples. We appreciate editorial assis-

tance provided by V.R. Beasley. Although some of

the research described has been funded in part by

National Oceanographic and Atmospheric Administra-

tion (NOAA) it has not be subjected to NOAA reviewand does not necessarily reflect the views of the NOAA,

and no official endorsement should be inferred.

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