Contaminant exposure and effects in pinnipeds: implications for Steller sea lion declines in Alaska

The Science of the Total Environment 311 (2003) 111–133

Contaminant exposure and effects in pinnipeds: implications for Steller sea lion declines in Alaska Mace G. Barrona,*, Ron Heintzb, Margaret M. Krahnc a P.E.A.K. Research, 1134 Avon Lane, Longmont, CO 80501, USA Auke Bay Laboratory, NOAAyNMFS, 11305 Glacier Highway, Juneau, AK 99801, USA c Northwest Fisheries Science Center, NOAAyNMFS, 2725 Montlake Boulevard East, Seattle, WA 98112, USA b

Received 26 September 2002; accepted 8 February 2003

Abstract After nearly 3 decades of decline, the western stock of Steller sea lions (SSL; Eumetopias jubatus) was listed as an endangered species in 1997. While the cause of the decline in the 1970s and 1980s has been attributed to nutritional stress, recent declines are unexplained and may result from other factors including the presence of environmental contaminants. SSL tissues show accumulation of butyltins, mercury, PCBs, DDTs, chlordanes and hexachlorobenzene. SSL habitats and prey are contaminated with additional chemicals including mirex, endrin, dieldrin, hexachlorocyclohexanes, tetrachlorodibenzo-p-dioxin (TCDD) and related compounds, cadmium and lead. In addition, many SSL haulouts and rookeries are located near other hazards including radioactivity, solvents, ordnance and chemical weapon dumps. PCB and DDT concentrations measured in a few SSL during the 1980s were the highest recorded for any Alaskan pinniped. Some contaminant exposures in SSL appear to be elevated in the Gulf of Alaska and Bering Sea compared to southeast Alaska, but there are insufficient data to evaluate geospatial relationships with any certainty. Based on very limited blubber data, current levels of PCBs may not pose a risk to SSL based on comparison to immunotoxicity tissue benchmarks, but SSL may have been at risk from pre-1990 PCB exposures. While exposure to PCBs and DDTs may be declining, SSL are likely exposed to a multitude of other contaminants that have not been monitored. The impacts of these exposures on SSL remain unknown because causal effects have not been established. Field studies with SSL have been limited in scope and have not yet linked contaminant exposures to adverse animal health or population effects. Several biomarkers may prove useful for monitoring exposure and additional research is needed to evaluate their utility in SSL. We conclude that there are insufficient data to reject the hypothesis that contaminants play a role in the continued decline of SSL, and suggest that a coordinated monitoring program be developed which can be related to key biological, ecological and laboratory toxicity data. 䊚 2003 Elsevier Science B.V. All rights reserved. Keywords: Sea lion; Contaminants; Marine mammal; Persistent organic pollutants

*Corresponding author. Tel.: q1-303-684-9646; fax: q1-303-479-9725. E-mail address: [email protected] (M.G. Barron). 0048-9697/03/$ - see front matter 䊚 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0048-9697(03)00140-2

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M.G. Barron et al. / The Science of the Total Environment 311 (2003) 111–133

1. Introduction The Steller sea lion (SSL; Eumetopias jubatus) is an endangered species and the National Marine Fisheries Service (NMFS) has the legal responsibility for restoring the affected populations in the United States. The western stock of SSL, which resides in the northern Gulf of Alaska (GOA), Aleutian Islands and Bering Sea, has experienced a severe decline in abundance since the first assessment surveys in the late 1950s and was listed as an endangered species in 1997 (Kruse et al., 2001; Loughlin and York, 2000). The cause of the steepest period of the decline in the western stock (1970s and 1980s) is attributed to low survival and low birth rates resulting from nutritional stress, as well as human caused deaths (Pitcher et al., 1998; Kruse et al., 2001; NMFS, 2001). A change in the availability of fatty forage fish such as herring to lower fat fishes such as walleye pollock (Theragra chalcogramma) was considered a major factor in causing nutritional stress. Pitcher et al. (1998) speculated that the major shift in the oceanic regime that occurred in the GOA during the late 1970s reduced the prey resources necessary to support a higher carrying capacity of SSL. Rosen and Trites (2000) fed captive SSL juveniles either herring or pollock diets and determined that the pollock-only diet resulted in weight loss and animals did not compensate for the lower energy content of the pollock. Declines in pollock populations in the GOA between 1984 and 1996 have lead Shima et al. (2002) to concluding that the decrease in prey density may have contributed to decreased foraging efficiency in SSL. During the 1990s, the overall rate of decline of juveniles and adults moderated, but overall population abundance has continued to decline at an estimated 5.2% per year (Loughlin and York, 2000). In comparison, the eastern stock of SSL in southeast Alaska (SEA) has been increasing at approximately 1.7% per year (Loughlin and York, 2000). Re-sighting studies (Raum-Suryan et al., 2002) also indicate lower survival in the western stock. The general scientific consensus is that the causes of the steep decline in the western stock of SSL in the 1980s are likely to be different from

the causes of the moderate rate of decline in the 1990s (ASLC, 2001). Despite the steep historical declines, Bickham et al. (1998) determined that the SSL population in the GOA had not lost appreciable genetic diversity. The cause of the recent declines in the western stock of SSL is unknown. Several hypotheses have been proposed to explain this continued decline in abundance. These include: (1) effects of commercial fishing on prey availability; (2) increased predation; (3) direct anthropogenic impacts such as harvest or harassment of SSL; (4) environmental change caused by climatic shifts resulting in alteration of the forage base for SSL; and (5) the effects of contaminants. Nutritional stress caused by a decline in prey availability is the leading theory of the current decline in the western stock of SSL, and is the basis for the biological opinion regarding limiting fisheries in proximity to SSL rookeries and haulouts (NMFS, 2001). However, the consensus of experts was that there was inadequate data to evaluate whether food limitation is a causative factor in the recent population declines in the western Aleutian Islands (ASLC, 2001). Additionally, NMFS (2001) concluded that there were no indications of nutritional stress in lactating females (1993–1997) or pups (1990–1996) at Aleutian Island study sites, nor signs of disease or malnutrition. There were insufficient data to support either competition with fisheries or natural predation (e.g. killer whales, sleeper sharks) as likely significant factors and anthropogenic impacts such as subsistence harvest and increased mortality from fishing were unlikely to account for current declines in SSL (NMFS, 2001). Loughlin and York (2000) analyzed trend site counts of non-pups and concluded that the majority (2.9– 3.8%) of the 5.2% annual decline in the western stock was due to unknown causes. Other factors have not been demonstrated to be causally linked to current declines, which suggests that other hypotheses including the potential for contaminant impacts should be evaluated. Consequently, the nutritional stress hypothesis remains to be demonstrated and competing hypotheses such as contaminants continue to be plausible. The objectives of this paper were to review and synthesize existing information on contaminants

M.G. Barron et al. / The Science of the Total Environment 311 (2003) 111–133

measured in SSL and their prey, and evaluate any associations between contaminant exposures and impacts. Contaminant exposure and effects in other Alaskan marine species, and in pinnipeds from other areas, were also considered because of limited information on SSL. Specific components of this paper include: (1) general spatial and temporal trends in North American marine mammals and birds; (2) contaminants and chemical groups resulting in exposures to Alaskan marine species (eagles, otters, murres, seals) that inhabit SSL habitats; (3) contaminant exposures in the diet and tissues of SSL; (4) chemical hazards located in proximity to SSL haulouts and rookeries; (5) contaminant toxicity in pinnipeds; (6) a preliminary risk evaluation from the comparison of tissue and dietary levels of contaminants in SSL to pinniped sublethal toxicity benchmarks; (7) potential biomarkers of exposure and effect that may be applicable to a SSL contaminants monitoring program; (8) data gaps that limit evaluations of the association between contaminant exposure and effects in SSL; and (9) research recommendations. 2. General trends in contaminant exposure in North American marine mammals and birds A wide range of persistent organic pollutants (POPs), heavy metals, radionuclides and hydrocarbon contaminants have now been repeatedly detected in marine mammals in northern latitudes. POPs are a group of halogenated contaminants that include: polychlorinated biphenyls (PCBs); polychlorinated dioxins and furans (PCDDs, PCDFs); hexachlorobenzene (HCB); and organochlorine pesticides such as ethanes (e.g. DDT), cyclodienes (e.g. chlordane, dieldrin), hexachlorocyclohexanes (HCHs), chlorinated camphenes (toxaphene), mirex and chlordecone (kepone). They are known for their environmental persistence and reproductive and developmental toxicity in birds and mammals (Barron et al., 1995). Contaminants are transported to Arctic and subArctic regions in the troposphere in gas phase, on particles, ocean currents and in migrating fish (Ewald et al., 1998; Muir et al., 1999; Zhang et al., 2001). Global contamination of POPs has been recognized since the 1980s, with surface water,

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air, fish and marine mammal tissues showing evidence of contamination in Arctic and subarctic environments (Iwata et al., 1993; Hutchinson and Simmonds, 1994; Tanabe et al., 1994; Muir et al., 1999; Weisbrod et al., 2000). Contaminants detected in Alaskan pinnipeds include PCBs, DDTs, chlordanes, HCHs, HCB, dieldrin, butyltins, arsenic, mercury, cadmium, lead and radionuclides (Hutchinson and Simmonds, 1994; Papa and Becker, 1998; Cooper et al., 2000; Woshner et al., 2001; Kucklick et al., 2002). In general, PCBs and DDTs in Arctic biota have declined over the last 20–25 years, but information on other POPs is more limited (AMAP, 1998). POPs in ringed seal (Phoca hispida) blubber and seabird eggs in the Canadian Arctic show declining PCBs and DDTs from the 1970s to the 1980s, then a leveling off by the early 1990s (Muir et al., 1999). Elevated PCBs in seals from sites near the Russian coast are consistent with continued use of PCBs in electrical equipment in Russia (Muir and Norstrom, 2000). Data are more limited for other POPs and significant declines over time are less apparent (Muir et al., 1999). Some contaminants may increase in Alaska marine mammals with continued use and translocation to Arctic regions from lower latitudes through global redistribution (Wania and Mackay, 1999). Ringed seal data from the Canadian Arctic are consistent with the ‘cold condensation’ hypothesis of increasing proportions of more volatile POPs with increasing latitude and distance from sources (Weis and Muir, 1997). More water soluble POPs like some HCH isomers are slower to accumulate in Arctic and subarctic food webs and may be increasing (Wania and Mackay, 1999). Mercury appears to be higher in more recent samples (mid 1990s) than in the 1980s and 1970s, and rates of Hg accumulation also appear to be higher than 10–20 years ago (Muir et al., 1999). Concentrations of polybrominated diphenyl ethers (PBDEs) also appear to be increasing in marine mammals (Ikonomou et al., 2002). Evaluations of spatial and temporal trends in POP levels in marine mammals are confounded by changes in analytical methodology and variability in animal geneticsyageysizeyreproductive status or dietary and population shifts (Hutchinson and

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Simmonds, 1994; Muir et al., 1999; O’Hara, 2001). 3. Contaminant exposures to marine animals in SSL habitats Contaminant exposures and impacts have been assessed in a variety of Alaskan mammals and birds that inhabit SSL habitats. Estes et al. (1997) and Anthony et al. (1999) studied productivity, diets and contaminants in nesting bald eagles from the western Aleutian Islands (WAI) in 1993 and 1994. Contaminants in eagle eggs included chlordanes, DDTs, dieldrin, HCB, HCHs, mirex, PCBs and heavy metals. Lower reproductive success of eagles on Kiska Island in the WAI was associated with higher levels of DDE, other POPs and Hg (Estes et al., 1997; Anthony et al., 1999). Estes et al. (1997) and Bacon et al. (1999) reported PCBs, PCDDs, PCDFs and chlorinated pesticides in sea otter livers from SEA, WAI and California collected between 1988 and 1992. DDTs, PCBs, chlordanes and dioxin toxicity equivalent quotients (TEQs) were 15–40 times greater in otters from the WAI than SEA, although differences may have been confounded with animal condition. Only PCBs were higher (1.6 times) in WAI otters compared to California otters and the source of contamination in the WAI was unknown (Bacon et al., 1999). Becker (2001) noted that preliminary comparisons of POPs and Hg in eggs of common (Uria aalge) and thick-billed (U. Lomvia) murres indicated higher levels of PCBs and 4,49-DDE and lower levels of HCB in GOA colonies than in eggs from the Bering Sea or eastern Canadian Arctic (Braune et al., 2001). Hg was higher in eggs collected from GOA colonies than in eggs from the Bering Sea, but lower than in eggs from eastern Canadian colonies (Becker, 2001). Chlordanes (0.098 mgykg fat), DDTs (1.8 mgykg), HCHs (0.24 mgykg), and PCBs (2 mgykg) were detected in subcutaneous fat of thick-billed murres collected from the North Pacific and Bering Sea in 1980 and 1982 (Kawano et al., 1986). In addition to these data, Stout et al. (2002) reported metal concentrations in the liver and kidney of four species of eiders from Alaska and arctic

Russia, but data were combined across all collection locations and could not be evaluated. Organochlorine contaminants (e.g. PCBs, pesticides) were either not-detectable or only present at trace levels in the eider tissues (Stout et al., 2002). An approximate 10-fold decline in POP exposure over a 25-year period is suggested by comparing northern fur seal blubber data for PCBs and DDTs collected in the 1990s and 1970s (Table 1). However, inconsistent with reports of 16–40 mgy kg of PCBs and DDTs in fur seal blubber in the 1960s and 1970s, Anas and Wilson (1970a) reported only trace levels of PCBs in the blubber of fur seal pups collected in 1969. Beckmen et al. (1999) reported that PCBs and DDTs in the blood of northern fur seal (Callorhinus ursinus) pups were similar in the milk of dams collected from the Pribilof Islands in 1995 and 1996 (Table 1). Lipid normalized concentrations of PCBs and DDTs in mother’s milk were greater than 40 times higher than in blood. Beckmen et al. (1999) concluded that northern fur seal pups have a substantial exposure to POPs at a critical stage of development, and exposure was higher in pups of primiparous dams than pups from multiparous dams. In contrast to trends in POP levels, Hg levels in fur seals from the Pribilof Islands appear to have increased between the 1970s and 1990s (Table 1) (Noda et al., 1995). Harbor seals (Phoca vitulina) have a similar distribution in Alaska as SSL, and their abundance has declined substantially over the last two decades in the GOA and Prince William Sound (PWS), which coincides with declines in SSL. For example, Frost et al. (1994) reported a 57% decrease in aerial counts of molting harbor seals in PWS between 1983 and 1992. Also, the diet of sea lions and harbor seals nearly completely overlapped in the GOA (Pitcher, 1981). Hypotheses for the decline in harbor seals include changes in food resources, human harvests, disease, increased predation, increased disturbance and pollution (Papa and Becker, 1998). Contaminants detected in harbor seals from PWS and the central GOA included DDTs, chlordanes, dieldrin, endrin aldehyde, HCHs, PCBs, cadmium, lead, mercury and selenium (Papa and Becker, 1998). HCH concentrations in blubber of harbor seals collected in 1993

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Table 1 Historical concentrations of contaminants in pinnipeds from the Bering Seaa Species

Tissue (ww)

Year collected

Life stageb

Contaminant (mgykg ww)

Source

Northern fur seal

Liver

1968

M, F

Anas and Wilson (1970b)

Blubber

1975 1992 1969

M, F M, F Pup

1968–1972

Pup

1990

M

1994–1996

Pup

Blood

1995, 1996

Pup

Hair

2000

Ringed seal

Blubber

1989–1995

Pup F M, F

Bearded seal

Blubber

1993–1995

M, F

PCBs: ND DDTs: 0.04 dieldrin: ND Hg: 10.7 Hg: 27"18 PCBs: ‘trace’ DDTs: 0.6–48 dieldrin: ND-0.09 DDTs: 16–40 PCBs: 22 PCBs: 1.3 DDTs: 2.7 Otherc: 0.05–0.8 PCBs: 1–2 DDTs: 2"1 PCBs: 0.2 DDTs: 0.008 Hg: 4.9 Hg: 7.8 PCBs: 0.09–0.4 DDTs: 0.07–0.3 Otherd: 0.004–0.9 PCBs: 0.05–0.4 DDTs: 0.008–0.4 Othere: -0.001–0.5

Noda et al. (1995) Anas and Wilson (1970a) Hutchinson and Simmonds (1994) Krahn et al. (1997) Beckmen et al. (unpublished) Beckmen et al. (1999) Beckmen et al. (2002) Krahn et al. (1997) Krahn et al. (1997)

a

Pribilof Islands or unspecified areas of the Bering Sea. ND: not detected (detection limit not specified); ww: wet weight. M: male; F: female (includes animals categorized as ‘subadult’). c Other: 0.8 mgykg chlordanes; 0.05 mgykg dieldrin; 0.0006 mgykg HCB. d Other: 0.09–0.3 mgykg chlordanes; 0.004–0.03 mgykg dieldrin; 0.007–0.05 mgykg HCB. e Other: 0.1–0.5 mgykg chlordanes; -0.001–0.009 mgykg dieldrin; 0.001–0.007 mgykg HCB. b

were nearly twofold higher at Kodiak Island (GOA) compared to SEA, whereas endrin aldehyde was higher in SEA harbor seals. Concentrations of chlordanes in blubber of harbor seals collected in 1993 were over twofold higher in PWS compared to SEA. Concentrations of HCB were similar in harbor seals from PWS and Washington and Oregon. Papa and Becker (1998) concluded from the limited data in harbor seals from Alaska that PCBs and DDTs were approximately 10 times lower than in seals from Washington and Oregon, and 100 times lower than in the highly contaminated seals of the Baltic Sea, southern coast of Norway and Dutch Wadden Sea. No contaminant data were available for harbor seals from the western GOA and WAI, and metals data

were only available for the central GOA (Papa and Becker, 1998). 4. Contaminant exposures in Steller sea lions There have been very few reports that document contaminant exposure in SSL and these have been generally limited in geographic scope and sample size. Table 2 summarizes concentrations of PCBs and DDTs in SSL blubber, and identifies other contaminants reported in each investigation. Ylitalo et al. (2001) previously discussed contaminant bioaccumulation and feeding ecology of SSL from Alaska, and noted that age, gender and reproductive status influenced POP tissue levels. DDTs and PCBs increased with age in male SSL, whereas

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Table 2 Contaminant concentrations in Steller sea lion blubber (mgykg wet weight) Collection year

Collection locationa

Age group

Gender

n

PCBs (mgykg)

DDTs (mgykg)

Other contaminantsb

Source

1976–1981

GOA

Juvenile to adult

Female

12

12.6"8.9

2.0"1.9

Chlordanes, HCHs, HCB

Lee et al. (1996)c,d

1985–1990

PWS, BS

Males Mixed

17 8

4.3"4.4 23"37

5.6"4.0 20"35

Chlordanes, others

Varanasi et al. (1992)d

1992–1994 1994–1998 1998–2000

SEA BS PWS SEA

Juvenile to adult Juvenile Juvenile Juvenile

Mixed Mixed Mixed

3 13 19 10

6.6"0.5 2.0"1.2 1.4"0.7 1.6"0.6

5.0"0.6 1.9"1.3 1.3"0.6e 1.4"1.1e

Chlordanes TEQ

Krahn et al. (1997) Krahn and Smolen (unpublished) Krahn et al. (2001)f

a

GOA: Gulf of Alaska; PWS: Prince William Sound; BS: Bering Sea; SEA: southeast Alaska. HCHs: hexachlorocyclohexanes; HCB: hexachlorobenzene; TEQ: toxicity equivalents for PCBs; others: unspecified chlorinated organics. c PCB and DDT data determined from mean lipid weight concentrations and mean % lipid values. d Also reports liver concentrations of contaminants. e p,p9-DDE. f Also reports feces concentrations from GOA, SEA and eastern Aleutian Islands. b

residues in female SSL increased to age 4 ( juveniles), then remained relatively constant from age 5 years and older (adults). This was attributed to female SSL reaching reproductive age and subsequent maternal transfer of residues to pups. Similar contaminant concentrations were observed in SSL from the western and central GOA, except for adult males. The available data indicated that PCBs and DDTs in samples collected in 1980s and 1990s were similar to or greater than in SSL collected in 1976–1978. Ylitalo et al. (2001) noted that some individual SSL from both the western and central GOA had blubber PCB levels approaching AMAP (1998) toxicity thresholds, which suggested the potential for adverse effects. Lee et al. (1996) estimated that approximately 80% of the total maternal body burden of PCBs and DDTs was transferred to SSL pups during lactation. Lee et al. (1996) concluded that PCB levels in male SSL were 1–2 orders of magnitude higher than those in ringed seals from Arctic waters, in northern fur seals from Alaska, and harp seals (Phoca groenlandica) from the Arctic and St. Lawrence. Varanasi et al. (1992) reported PCB and DDT concentrations measured in a few SSL during the 1980s that were the highest recorded for any Alaskan pinniped, with a blubber concentration of 96 mg PCBykg (wet weight; ww) in

one juvenile male collected in the Bering Sea in 1985. Krahn et al. (2001) reported contaminant levels in blood, blubber, feces and prey of SSL collected from SEA and GOA during 1998–2000. They also performed health assessments of SSL and determined porphyrin profiles in feces as a biomarker of POP exposure. They noted a greater frequency of dermal fungal patches in eastern Aleutian Island (EAI) SSL, and suggested that the western stock may have greater immunosuppression than SEA SSL. Lipid normalized concentrations of TEQ, DDTs and PCBs (sum of selected congeners) in feces were 1.3–2 times higher in the EAI than in the SEA, but only PCBs were significantly elevated. TEQ, DDTs and PCBs in SSL feces from the SEA were 1.9–2.5 times higher than in central GOA SSL. PCBs, p,p9-DDE, and TEQ were not significantly different in blubber of SEA and PWS SSL, but sample sizes were small. Blood levels of selected PCB congeners and DDTs were highly correlated with blubber when reported on a lipid basis, suggesting that blood sampling may be a suitable alternative to blubber biopsy of POPs in SSL. However, blood concentrations should be interpreted with caution because contaminant levels in blood vary significantly with fasting and molting in other species of pinnipeds (Lydersen et

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Fig. 1. Mean PCBs and DDTs in blubber (mgykg ww) of juvenile (1–5 y) Steller sea lions collected in Alaska between 1976 and 2000 (ns2–19). Error bars are 1 S.D.. BS: Bering Sea; GOA: Gulf of Alaska; PWS: Prince William Sound; SEA: southeast Alaska. PCB blubber data from Varanasi et al. (1992), Lee et al. (1996), Krahn et al. (2001) and Krahn (1997) and Krahn and Smolen (unpublished).

al., 2002). Lipid normalized feces concentrations of POPs were not correlated with blubber, suggesting that feces were indicative of more recent dietary exposures. Krahn et al. (2001) reported higher ratios of coproporphyrin III to urophorphyrin ratios in EAI SSL in SSL from SEA and PWS. They also reported a positive correlation with PCB concentrations in feces in POPs, which can be influenced by animal conditions. They suggested that the porphyrin results indicated possible inhibition of a component of the heme synthesis pathway (coproporphyrin oxidase) and may be a biomarker of POP exposure in SSL. The only investigations of metal exposures in Alaskan SSL are those of Kim et al. (1996) and Beckmen et al. (2002). Kim et al. (1996) reported butyltin compounds in SSL liver collected in the GOA between 1976 and 1985, and from Hokkaido, Japan during 1994 to 1995. Mean total butyltin compounds in liver of SSL from Alaska was 19 ngykg (ww) which was approximately 10-fold lower than in SSL from Japan. Total butyltins in GOA SSL were similar across gender and age, and no temporal trend was evident. Beckmen et al. (2002) reported significantly higher Hg in fur

of SSL of mixed gender from PWS ( juvenile: 4.9 mgykg ww; pup: 1.7 mgykg) than from SEA SSL ( juvenile: 0.6 mgykg; pup: 1.1 mgykg). A single muscle sample from an SSL from the Aleutian Islands had a Hg concentration of 1.7 mgykg (unpublished data of Duffy cited in Beckmen et al., 2002). A consistent set of data for PCBs and DDTs in juvenile SSL blubber (wet weight) was compiled and presented in Fig. 1 because these are the only contaminants monitored over a broad time period and substantial portion of the range of SSL in Alaska, and contaminant concentrations are less affected by gender in juvenile SSL. Juveniles were defined as less than 6 years old based on an average age of first pregnancy of 4.9"1.2 years in GOA SSL studied between 1975 and 1976 (Pitcher and Calkins, 1981). Fig. 1 suggests a general decline in exposure to PCBs and DDTs over the last 12 years, and similar exposure in the western stock (GOA, Bering Sea, PWS) and SEA. However this figure is based on relatively limited data: only 70 data points over a 25-year period and over 2000 miles in longitude that encompass SSL habitat. There was insufficient information to

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evaluate temporal and spatial trends for other contaminants. Additionally, PCB trends may be confounded with changes in analytical methodology because prior to the mid-1980s total PCBs were determined from a comparison to Aroclor mixtures which may overestimate PCB concentrations in blubber (R. Addison, personal communication). Also, spatial and temporal trends may be influenced by animal condition (e.g. blubber thickness), but this information was not available in the reported datasets. Information on contaminants in SSL prey are also limited in sample size, geographic scope and the number of contaminants analyzed. de Brito et al. (2002) reported POPs in the liver of walleye pollock in the Bering Sea (three locations) and GOA (three locations) collected during 1992. Pollock were the predominant prey consumed by SSL in the central Bering Sea and GOA as determined in surveys performed between 1975 and 1981 (Calkins, 1998; Pitcher, 1981). However, feeding differences are apparent based on stable isotope analysis (Ylitalo et al., 2001). For example, adult female and male SSL from the Bering Sea and juvenile males from western GOA fed at a higher trophic position than adult and other juveniles from the western and central GOA (Ylitalo et al., 2001). Mean POPs in Bering Sea pollock ranged from: 0.4 to 1 mg PCBsykg lipid; 0.3–0.5 mg DDTsykg; 0.2 mg chlordanesykg; 0.07–0.08 mg HCHsykg; and 0.06–0.1 mg HCBykg lipid (de Brito et al., 2002). Mean POPs in GOA pollock ranged from: 0.3 to 2 mg PCBsykg lipid; 0.1–0.6 mg DDTsykg; 0.08–0.2 mg chlordanesykg; 0.05– 0.08 mg HCHsykg; and 0.02–0.05 mg HCBykg lipid (de Brito et al., 2002). Kawano et al. (1986) reported PCBs (0.41 mgykg), DDTs (0.35 mgy kg), chlordanes (0.14 mgykg), and HCHs (0.21 mgykg) in lipid of pollock collected from the Bering Sea in 1982. de Brito et al. (2002) noted that PCB concentrations appeared to have increased in Bering Sea pollock, and there was no evidence of a decrease in DDTs and chlordanes (de Brito et al., 2002). de Brito et al. (2002) concluded that concentrations were relatively low compared to North Atlantic and European countries. A limited analysis of additional SSL prey fish indicated that concentrations of PCBs and

DDTs were not significantly different in the Bering Sea, EAI and GOA (Krahn et al., 2001). Zhang et al. (2001) reported mean total Hg in salmon muscle returning via the Bering Sea in 1999 and 2000 of 0.034–0.096 mgykg (ww) and Easton et al. (2002) reported levels of 0.056 and 0.026 mgy kg (ww) for salmon collected from an unspecified location in Alaska. Salmon can be an important prey item of SSL foraging in the EAI and along the Alaska peninsula in summer (Sinclair and Zeppelin, 2002). Ewald et al. (1998) reported sockeye salmon returning to the Copper River arrived with PCB concentrations of 0.67 mgykg in muscle lipids and DDT concentrations of 0.22 mgykg in muscle lipids. 5. Chemical hazards in proximity to SSL Potential chemical hazards located in proximity to SSL haulouts and rookeries were evaluated using Geographic Information System (ArcView 8.1) mapping of SSL locations, site population trends, and hazardous chemical sites. Chemical hazards in proximity to SSL locations were determined by evaluating publicly available information on formerly used defense sites (Army Corps of Engineers FUDS online database), sites described in the Alaska Department of Environmental Conservation’s Contaminated Site Database and other information sources. Chemical hazards were grouped into one of six general categories based on the type of contaminantypotential hazard (Table 3). Population trend data were obtained from the NMFS National Marine Mammal Laboratory and the Alaska Department of Fish and Game. Figs. 2–5 show that multiple chemical hazards exist in close proximity to SSL haulouts and rookeries, including sites containing PCBs, PAHs, metals, ordnance and chemical weapons, radioactivity and other contaminants. Figs. 2–5 depict recent population trends (increasing, stable, declining) at each SSL location with trend data, and generally show that the western stock (PWS, GOA, Bering Sea) have a greater prevalence of negative trend data than the eastern stock. These figures also show that haulouts or rookeries in close proximity to each other (e.g. within 5 km) can show widely different population trends. For exam-

M.G. Barron et al. / The Science of the Total Environment 311 (2003) 111–133 Table 3 Categories of potential chemical hazards used in GIS mapping of SSL and hazard locations Category

Types of materials included

PAH

Lubricants, Bunker C, heating oil, diesel fuel, fuel oil, creosote, gasoline gasoline Polychlorinated biphenyls, Electrical equipment Heavy metals, lead paint, mine tailings, batteries Mustard gas, lewisite (three sites) Evidence of radioactivity (one site) Pentachlorophenol, chlorinated solvents, antifreeze, ordnance landfill seeps

PCB Metals Chemical weapons Radioactive Miscellaneousa

a

Separate databases combined into miscellaneous category for display purposes.

ple, Fig. 3 shows that some haulouts on Atka Island have greater than 12% declines, while others show an increasing population trend. Trend data may require a higher level of ordering, such as the metapopulations described by York et al. (1996). These maps indicate that SSL may be exposed to multiple types of contaminants that have not been analyzed in SSL tissues and prey. 6. Organic contaminant toxicity in pinnipeds Effects reported in pinnipeds exposed to elevated levels of POPs have included skeletal deformities, adrenal gland pathology, uterine blockage, impaired reproduction, P450 induction, immunotoxicity, and modulation of retinol (vitamin A) and thyroid hormone levels (Hutchinson and Simmonds, 1994; Addison, 1989; O’Hara and O’Shea, 2001; Ross and Troisi, 2001). For example, there was an increased prevalence of skull bone lesions in Baltic gray seals (Halichoerus grypus) after 1960 than in seals collected before 1950 (Bergman et al., 1992). Bergman et al. (1992) suggested that the lesions may have been caused by hormone imbalance and immune deficiency, and that the increase in lesions coincided with increased levels of PCB and DDT in Baltic biota. The available field investigations of SSL (e.g. Krahn et al., 2001, discussed above) have not yet established a causal

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link between contaminant exposure levels and declining populations of SSL or other adverse effects. Adverse effect levels of contaminants in SSL are unknown, and must be inferred from studies in other species of pinnipeds or sensitive terrestrial species such as mink. Table 4 summarizes adverse effects levels of PCBs and DDTs derived from a review of laboratory feeding studies in harbor seals and field investigations conducted in contaminated areas (e.g. Baltic Sea, Dutch Wadden Sea). For the majority of these studies, adverse effects have been attributed to PCBs, rather than DDT, but interpreting contaminant impacts only from field data can be difficult because of confounding factors such as nutritional and reproductive status. Addison (1989) and Papa and Becker (1998) have previously provided a critical review of several of these studies, as well as investigations of cetaceans, and generally concluded that causal linkages could not be established. The toxicity of organic contaminants other than PCBs and DDTs to pinnipeds have not been reported. An additional uncertainty is the presence of complex mixtures of contaminants, and the limited set of analytes currently quantified in SSL. Adverse effect levels determined from laboratory feeding studies and field investigations ranged from 16.5 to 704 mg PCBykg blubber (lipid weight) of PCBs and 2.4–824 mg DDTykg blubber (Table 4). However, field investigations have been unable to establish a causal link between contaminant exposures and reproductive impairments in pinnipeds that is not confounded with other factors (e.g. epizootics, nutrition) (Addison, 1989; Papa and Becker, 1998). For example, results of the first captive feeding study with harbor seals fed Dutch Wadden Sea fish agree with field observations of impaired reproduction in the Wadden Sea seals, but could not be unambiguously interpreted because control seals were fed different species of fish that differed in caloric content (Addison, 1989). Also, there was a strong correlation between PCB blubber lipid concentrations over 70 mgykg and uterine occlusions in sexually mature female ringed seals from the Baltic Sea (Helle et al., 1976a,b). However, it was uncertain whether PCBs caused the occlusions or

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Fig. 2. Map of Alaska showing locations of potential contaminant hazards in areas of Steller sea lion haulouts and rookeries. Boxes indicate larger scale maps for Near and Rat Islands (A); Andreanof Islands (B); Fox Islands (C); Shumagin Islands and Alaskan Peninsula (D); Kodiak Island and Kenai Peninsula (E); Prince William Sound (F); and Southeast Alaska (G). Only large scale maps (B) (Fig. 3); (C) (Fig. 4); and (G) (Fig. 5) are provided below.

Fig. 3. Proximity of Steller sea lion rookeries and haulouts to potential contaminant hazards in the western Aleutian Islands (Andreanof Islands; Map B of Fig. 2). The figure shows recent population trends (increasing, stable, declining) at each SSL location with trend data.

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Fig. 4. Proximity of Steller sea lion rookeries and haulouts to potential contaminant hazards in the central Aleutian Islands (Fox Islands, Map C of Fig. 2). The figure shows recent population trends (increasing, stable, declining) at each SSL location with trend data.

Fig. 5. Proximity of Steller sea lion rookeries and haulouts to potential contaminant hazards in southeast Alaska (Map G of Fig. 2). The figure shows recent population trends (increasing, stable, declining) at each SSL location with trend data.

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whether a lack of reproduction due to uterine occlusions could elevate contaminants in affected animals by not allowing depuration by reproduction and lactation (Addison, 1989). The clearest causal linkage between contaminant exposure and adverse effects in pinnipeds were observations of immunotoxicity in juvenile captive harbor seals fed herring from the Baltic Sea (4.4 mgykg lipid) for 2.5 years (de Swart et al., 1996; Ross et al., 1995, 1996). The control group was fed a nutritionally comparable diet of less contaminated herring from the Atlantic Ocean (0.88 mgy kg lipid). Seals fed Baltic herring exhibited suppression of in vitro natural killer cell activity and specific T-cell responses and in vivo impairment of delayed-type hypersensitivity and antibody responses. These observations consistently indicated that contaminants in the Baltic herring affected cellular immunity rather than humoral immunity in seals (Ross et al., 1995; de Swart et al., 1996). Although DDTs and other contaminants were present in the Baltic herring, the authors concluded that PCBs, particularly planar (mono- and nonortho substituted) congeners, were responsible for the observed immunosuppression (Ross et al., 2000; Ross, 2002). Lines of evidence implicating planar PCBs included (Ross et al., 1995, 1996, 2000; Ross, 2002): (1) immunotoxicity in captive seals was consistent with dioxin-like toxicity; (2) PCBs contributed 93% of TEQ; and (3) rat studies using identical herring diets and a positive control group exposed to TCDD confirmed that dioxinlike PCBs were primarily responsible. Based on TEQ analyses, PCBs were implicated rather than PCDDsyPCDFs (Ross et al., 1995). The adverse effect levels for both total PCBs and TEQ reported in the captive harbor seal study were also consistent with adverse effects levels in free-ranging harbor seals (Simms et al., 2000) and in the Dutch Wadden Sea feeding study (Boon et al., 1987; Brouwer et al., 1989; Reinjders, 1986). Ross et al. (1995, 1996) reported immunosuppression in the captive harbor seals fed Baltic herring at a mean TEQ of 209 ngykg blubber (16.5 mg total PCBsykg), whereas the control group was fed herring containing 62 ngykg TEQ (6.9 mg total PCBsykg). Consistent with these adverse effect concentrations, Simms et al. (2000) reported

that harbor seal pups from Washington State, USA with elevated blubber PCBs (15 mgykg) and TEQ (154 ngykg) had significantly lower blood retinol than pups from British Columbia, Canada (2.3 mg PCBykg; 53 ng TEQykg). Mean blood levels of PCBs in the captive harbor seals were 7.1 mgykg lipid (controls) and 15 mgykg (immunosuppressed Baltic group) (de Swart et al., 1996; Ross et al., 1995, 1996). Similar blood levels of PCBs (25– 27 mgykg) in the seals that exhibited lower pregnancy and lower plasma retinol and thyroid hormone levels were observed in the Wadden Sea feeding study (Brouwer et al., 1989; Reinjders, 1986). Blood levels of PCBs (5.2–11 mgykg lipid; Brouwer et al., 1989; Reinjders, 1986) in the control seals in the Wadden Sea study were also consistent with the captive harbor seal study of Ross et al. (Boon et al., 1987). 7. Metal toxicity in pinnipeds Contaminant investigations of metals in pinnipeds have been limited to dose–response studies of Hg in harp seals (Ross and Troisi, 2001) and Sonne-Hansen et al. (2002) recently reported that there was no toxicity attributable to cadmium in the kidney of ringed seals at concentrations as high as 248 ugyg (ww). Ronald et al. (1977) and Ramprashad and Ronald (1977) orally dosed three groups of harp seals (two animals per group) with either 0, 0.25, or 25 mgykg body weight per day of methylmercury (MeHg). Both seals died in the 25 mgykg*d group within 26 days of exposure, and reduced appetite, weight loss, and damage to sensory epithelium of the cochlea occurred in the 0.25 mgykg*d group within 60 days of exposure. Hg levels reported in migrating salmon were low (0.034–0.096 mgykg ww; Zhang et al., 2001) and were below effects levels in sensitive mammalian species. Based on anticipated dietary intakes in pinnipeds, fish were considered unlikely to be sufficiently contaminated to cause MeHg toxicity except in pinnipeds from the most polluted areas (Ross and Troisi, 2001). Papa and Becker (1998) have cautioned against interpreting risks of metals in marine mammals from toxicity benchmarks

Species

Location

Ageysex

PCBs (mgykg lipid)

DDTs (mgykg lipid)

Effects

Source

California sea lion (Zalophus californianus) Ringed seal (Phoca hispida) Harbor seala (Phoca vitulina) Harbor sealb,c

Channel Islands, CA

Adult female

e: 124 ne: 17

e: 824 ne: 103

Pre-mature parturition

DeLong et al. (1973)

Baltic Sea, Gulf of Bothnia Wadden Sea, Netherlands UK

Adult female

Helle et al. (1976a) Helle et al. (1976b) Reinjders (1980)

Death from 1988 epizootic

Hall et al. (1992)

Lab feeding study

e: 130 ne: 88 e: 47 ne: 8.5 e: 3.4 ne: 1.0 not reportede,f

No pregnancy, uterine lesions Low reproductive rate

Harbor seal

e: 110 ne: 73 e: 701 ne: 76 e: 20 ne: 5.2 e: ;26e,f

Lower plasma retinol and thyroid hormones, lower pregnancy rate

Brouwer et al. (1989) Reinjders (1986) Boon et al. (1987)

ne: ;8e,f

not reportede,f

e: 16.5g ne: 6.9

e: 2.4 ne: 0.3

Impaired immunity

de Swart et al. (1996)

Adults (both genders) Mixed ages and gender Adult female

(Wadden Sea plaice) Harbor seald a

Lab feeding study (Baltic herring)

Juvenile

No effect concentrations determined in seals from Germany and Denmark. Effect concentrations determined from dead seals, which may result in artefactual elevation of contaminant levels. c Sites included: The Wash, M. Firth and W. Coast. e: Dead; ne: live (survived epizootic). d Effects linked to planar PCBs (effect level: 209 ng TEQykg blubber; no effect: 62 ngykg), not DDTs. e Concentration in blood lipids; blubber concentrations not reported. f ICES (1998) cites unpublished data of J. Boon: significant reproductive effects at estimated wet weight blubber concentrations of 10–15 mgykg PCBs and 2–3 mgykg DDTs. g Indicates absence of confounding factors and causal link between contaminant and toxicity. e: Effect level; ne: no effect level. b

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Table 4 Mean concentrations of PCBs and DDTs in blubber that have been associated with toxicity in pinnipeds (mgykg lipid weight)

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established in terrestrial animals because of possible greater tolerance in marine mammals. 8. Preliminary risk evaluation of PCBs in SSL The concentrations of PCBs in diet, blubber and blood determined to cause immunotoxicity in captive harbor seals are considered to be appropriate benchmarks for evaluating risks to SSL. Reasons include the consistency in dietary toxicity between the Wadden Sea and Baltic feeding studies, an appropriate sublethal endpoint (immunotoxicity) and causal link to adverse effects in pinnipeds. SSL also exhibited in vitro immunotoxicity (modulation of lymphocyte proliferation) from selected PCB congeners (De Guise and Levin, 2001), indicating the appropriateness of an immunotoxicity benchmark for SSL. Ross (2002) concluded that bioaccumulative immunotoxic chemicals may facilitate the emergence of infectious diseases in marine mammals by reducing host resistance, increasing virus production within individuals, and increasing rates of transmission within and among populations. Moderate levels of immunosuppression may not have biological consequences until a population is faced with an epizootic (Muir et al., 1999). A preliminary assessment of risks of PCBs in SSL was performed by comparing available exposure data (e.g. PCBs in blubber and diet) to immunotoxicity benchmarks derived in captive harbor seals. The immunotoxicity benchmark of 16.5 mg PCBykg blubber (lipid weight) was adjusted to a wet weight concentration of 7.8 mg PCBykg blubber (ww) using a mean percentage lipid in SSL blubber of 47.3% (Krahn, unpublished data). Fig. 6 compares juvenile PCB data (from Fig. 1) to the immunotoxicity benchmark, and suggests that current levels of PCBs in SSL are unlikely to pose a risk. Fig. 6 also suggests that historical PCB exposures may have posed a risk to SSL because trend data indicate levels exceeding the immunotoxicity benchmark existed prior to 1990. However, as noted previously, the data are extremely limited relative to the large geographic and temporal scope of the assessment. Also, analytical methods differed between the 1990s (sum of congeners) and earlier analyses

Fig. 6. Comparison of mean PCBs in blubber (symbols) of juvenile (1–5 y) Steller sea lions (see Fig. 1 for details) to an immunotoxicity benchmark (dashed line; derived from de Swart et al., 1996; see text).

(comparison to Aroclor standards which may overestimate PCB concentrations in blubber). Consistent with Fig. 6, PCB levels in male SSL (1–12 years old) collected in the GOA between 1976 and 1981 had PCB levels w4.2–30 mgykg (ww); derived from Lee et al., 1996x that exceeded the immunotoxicity benchmark (7.8 mgykg ww). In contrast, PCBs in female SSL (2–25 years old; Lee et al., 1996) had lower mean (3.9 mgykg) and maximum (11.8 mgykg) concentrations, indicating lower risk because of maternal transfer of contaminant burdens to pups. Dietary exposure data for SSL that are appropriate for risk assessment are even more limited than data on contaminant levels in SSL tissue. de Brito et al. (2002) reported that mean PCB concentrations in Bering sea and GOA walleye pollock collected in 1992 ranged from 0.18 to 3.2 mgykg lipid. Pollock are the main prey of SSL and PCB levels approached but did not exceed the dietary immunotoxicity benchmark of 4.4 mgykg lipid (de Swart et al., 1996). However, while pollock are the major component of SSL diets, pollock may not be the largest source of lipid intake in SSL. Salmon have higher lipid content and can also be important prey for the western stock (Sinclair and Zeppelin, 2002). However, the few reports of PCB and DDT

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levels in salmon (Easton et al. 2002; Ewald et al. 1998) indicate similar contaminant loads to pollock. Other fish species that may contribute a substantial portion of lipid in SSL diets include eulachon, herring, capelin and sandlance, but contaminant exposure in these fish species is unknown. 9. Biomarkers of exposure and effect in pinnipeds Biomarkers are biochemical, physiological, or histopathological indicators of exposure andyor effects of anthropogenic substances at the suborganismal or organismal level (Anderson et al., 1997). Biomarkers that have been measured in pinnipeds include P450 induction, immunological parameters, thyroid hormone and retinol levels, porphyrin compounds and metallothionein (Addison, 2001; Ross and Troisi, 2001). Additionally, Atkinson et al. (2001) are investigating stress hormone levels in SSL. Table 5 summarizes biomarkers that have been measured in pinnipeds to evaluate the exposure and effects of contaminants. The monooxygenase enzyme, cytochrome P4501A, is induced from exposure to planar halogenated aromatic hydrocarbons and has been the most frequently used biomarker in pinnipeds. P450 induction has not been determined in SSL, but cDNA fragments of SSL have been classified in the CYP1A1 and CYP1A2 subfamilies of P450 (Teramitsu et al., 2000). Kim and Hahn (2002) reported that the affinity of the aryl hydrocarbon receptor for TCDD in harbor seals was similar to the mouse, suggesting potential similar sensitivity to dioxin-like compounds. Despite recognized utility as a biomarker of planar hydrocarbon exposure in other species, the appropriateness of monitoring P450 induction in SSL is unclear because of variable responses in seal species (Chiba et al., 2002; Wolkers et al., 2002). Various indicators of immune effects have been monitored in SSL and other pinnipeds, including health assessments, in vitro assays and captive feeding studies (Table 5). Ross (2002) discussed pinniped immunology and the potential role of pathogens and POP-related immunotoxicity in infectious disease outbreaks in marine mammals.

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Contaminants were considered to have a role in epizootics involving California sea lions (Zalophus californianus), harbor and gray seals in northern Europe, Baikal seals, striped dolphins in the Mediterranean Sea, harbor porpoises in the United Kingdom, common dolphins in the Black Sea, and Caspian seals. Antibodies have been monitored in SSL blood, and monitoring of immunoglobulins has been initiated (Atkinson et al., 2001). Thyroid hormone levels are modulated by a variety of POPs, including PCBs (Brouwer et al., 1989; Barron et al., 1995). Thyroid levels have been determined in other pinniped species, but have not been reported in SSL. Hall et al. (1998) and Addison (2001) have concluded that the utility of monitoring thyroid hormone levels in pinnipeds is compromised by the considerable natural variation in T3 and T4 levels and variable responses to contaminants (Table 5). Retinol and its metabolites regulate a wide variety of physiological functions, including growth and development, and studies suggest that exposure to complex environmental mixtures of PCBs and PCDDsyPCDFs can disrupt vitamin A physiology and alter dynamics in marine mammals (Simms and Ross, 2000). Retinol levels have been determined in other pinniped species but have not been reported in SSL. Circulatory retinol is the least invasive vitamin A biomarker but appears to have variable response to contaminant exposure (Simms and Ross, 2000) (Table 5). Retinol is transferred via the placenta and lactation, which may confound biomarker monitoring in pinniped pups. Other biomarkers measured in pinnipeds include porphyrins and metallothionein (Table 5). Porphyrins are components of the heme synthesis pathway for the formation of blood hemoglobin and have been measured in SSL and other pinnipeds (Table 5). Porphyrin compounds have been monitored in SSL feces and have been suggested as a noninvasive biomarker of contaminant exposure in endangered pinnipeds (Fossi et al., 1997a). Metallothionein is a biomarker of metal exposure but has received limited evaluation in pinnipeds, in part because of the requirement for invasive measurements such as liver samples (Table 5).

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Table 5 Biomarkers used in monitoring contaminant exposure and effects in pinnipeds Biomarker

Species

Observation

Source

P450 (CYP1A in liver)

Harp seal

Maternal transfer of PCBs and chlorinated pesticides did not result in P450 induction in pups Significant correlation of P450 activity with TEQs (4.9 to 120 ngykg), coplanar PCBs and total PCBs No P450 induction, despite similar contaminant levels in blubber as ribbon seal P450 activity from a contaminated harbor in Argentina appeared to be elevated. Skin biopsy method developed. P450 content and activity were correlated with total PCBs in blubber P450 characterization and monitoring Noted a greater frequency of dermal fungal patches in EAI SSL Determined antibody presence of some microbial disease agents in SSL collected between 1978 and 1996 Monitoring the immunoglobulins IgG, IgM, IgA and cortisol in blood performed in vitro assays of lymphocyte proliferation in blood samples from mice, SSL and other marine mammals. Reported skin lesions and alterations in blood chemistries in seals exposed to PCBs and DDTs. Seals fed contaminated fish exhibited in vitro and in vivo immunosuppression Negative correlation between plasma T3 and increased di-ortho PCBs Negative correlation between T3 and POP levels No significant relationship between PCB exposure and thyroid hormone concentrations No correlation between thyroid hormone levels in pups and PCB concentrations in blood; ratios of total T4 to free T4 in blood were negatively correlated Plasma T3 and T4 were reduced in captive harbor seals consuming 1.5 mg PCBs per day T4 levels in blood were negatively correlated with blubber contaminants (TEQ) in captive seals Significantly lower serum T3 and T4 in diseased juvenile seals with elevated serum levels of PCBs and DDTs than in normal seals Seals fed diets containing 1.5 mgyd PCBs had lower plasma retinol

Wolkers et al. (2002)

Ribbon seal

Southern sea lion Harbor seal

Immunological parametersyhealth assessments (blood, saliva, skin)

SSL

Northern elephant seals Harbor seal Thyroid hormones (blood)

Largha seala Ribbon seal Grey seal

Harbor seal

Elephant seal

Retinol (blood)

Harbor seal

Fossi et al. (1997a) Fossi et al. (1997b) Troisi and Mason (1997) Addison et al. (1986) Krahn et al. (2001) Sheffield and Zarnke (1997) Atkinson et al. (2001) De Guise and Levin (2001) Beckmen et al. (1997) Ross et al. (1995) de Swart et al. (1996) Chiba et al. (2001) Hall et al. (1998) Jenssen et al. (1995) Brouwer et al. (1989) P. Ross (unpublished; cited in Addison, 2001) Beckmen et al. (1997) Brouwer et al. (1989)

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Largha seala

Chiba et al. (2002)

Table 5 (Continued) Biomarker

Species

Grey seal Elephant seal

Metallothionein (liver) a

SSL

Southern sea lion Harp seal

Possible subspecies of harbor seals.

Source

Positive correlations between contaminant burden and total circulatory retinol Blood retinol levels in pups was negatively correlated with PCB concentrations in blood Significantly lower serum retinol in diseased juvenile seals with elevated serum levels of PCBs and DDTs, than in normal seals Some elevation of Coproporphyrin III and higher ratios of coproporphyrin III to urophorphyrin with increasing PCB concentrations in feces Total porphyrin levels were correlated with Hg in fur of sea lions Pups had similar MT levels as their mothers and MT levels generally increased with age in older (10q years) adults

Simms et al. (2000) Jenssen et al. (1995) Beckmen et al. (1997) Krahn et al. (2001) Fossi et al. (1997a) Wagemann et al. (1992)

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Porphyrins (feces)

Observation

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10. Discussion The existing contaminant data for SSL in Alaska are extremely limited, and are based on small sample sizes, few historic or current samples, few analytes and inconsistent data sets (e.g. different tissues, locations, age classes, analytes). For example, Fig. 1 is a compilation of available PCB and DDT data for juvenile SSL, and is based on relatively limited data: only 70 data points over a 25-year period and over 2000 miles in longitude that encompass SSL habitat. There was insufficient information to evaluate any temporal and spatial trends for other contaminants in SSL. These data gaps impair our ability to evaluate temporal trends in exposure and whether contaminant exposures differ significantly between western and eastern stocks of SSL. Additionally, often key ancillary information (e.g. specific collection location; SSL age, reproductive status, blubber thickness) which is known to affect contaminant levels and healthy biomarker measurements in pinnipeds have not been presented in reports and articles. Marine birds and mammals inhabiting SSL habitats are exposed to a variety of contaminants, and concentrations may be higher in the GOA than in SEA. Harbor seal and sea otter populations have experienced substantial declines in abundance as have SSL. It is unclear if the cause of the declines is related to contaminants. It is also unclear if declines in harbor seals and SSL are linked. The limited available information indicates that SSL have accumulated butyltins, mercury, PCBs, DDTs, chlordanes and HCB. PCB and DDT concentrations measured in a few SSL from the Bering Sea and GOA in the 1980s were the highest measured in any Alaskan pinniped. SSL habitats and prey are contaminated with additional chemicals including mirex, endrin, dieldrin, HCH, dioxin compounds (PCDDsyPCDFs), cadmium and lead. SSL haulouts and rookeries are in proximity to chemical hazards including sources of PCBs, PAHs, heavy metals, radioactivity, solvents, ordnance and chemical weapons. Some contaminant exposures in SSL appear to be elevated in the GOA and Bering Sea compared to SEA, but there are insufficient data to evaluate geospatial trends with any certainty. Contaminant exposures in SSL

appear to have decreased since the 1980s, but there are insufficient data to evaluate temporal trends with any certainty. Additionally, some contaminants such as Hg appear to be showing little decline or may be increasing. SSL may also be exposed to a multitude of potential contaminants that are not monitored. For example, the flame retardant compounds PBDEs have increased 10to 100-fold in blubber of harbor seals collected near San Francisco Bay over the last decade (She et al., 2002). PBDE congeners are bioaccumulative, and can cause thyroid hormone disruption, neurodevelopmental effects and possibly cancer (MacDonald, 2002). MacDonald (2002) concluded that continued use of PBDEs in consumer products (e.g. 18.5 million pounds of penta-BDEy year in Americas) will result in increasing tissue concentrations in some populations. Ikonomou et al. (2002) reported PBDEs had exponentially increased in ringed seals from the Canadian Arctic between 1981 and 2000, and that PBDEs may become the most prevalent POP in arctic ringed seals in the next 50 years. Thus, a significant data gap in our understanding is the potential for unmeasured contaminant exposures in SSL, many of which may be increasing. Contaminant toxicity and risks are largely unknown in SSL and are little understood in pinnipeds in general. Definitive studies that have causally linked contaminant exposures and adverse effects in pinnipeds have been limited to laboratory studies with PCBs and Hg in dietary studies with captive seals. Field studies with pinnipeds have been confounded with other factors, and can not be unambiguously linked to contaminant caused impacts. The relative sensitivity of pinnipeds to contaminants compared to other species is largely unknown and adverse effect levels of contaminants in SSL must be inferred from studies in other species. The concentrations of PCBs in diet, blubber and blood determined to cause immunotoxicity in captive harbor seals were determined to be appropriate benchmarks for evaluating sublethal PCB risks to SSL. Based on very limited blubber data, current levels of PCBs may not pose a risk to SSL. SSL may have been at risk from pre-1990 PCB exposures based on historic blubber data. PCB levels

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in pollock collected in 1992, which are the main prey of SSL, did not exceed sensitive dietary toxicity levels but these data are limited. Also, contaminants in other prey items that may serve as important sources of dietary lipids in SSL are unknown. The risks of contaminant exposure and impacts in SSL are not understood because of uncertain or unknown exposures (e.g. only PCBs and DDTs are monitored with any frequency) and unknown toxicity. For example, Papa and Becker (1998) noted that toxaphene levels have been discovered in beluga whales from the Alaskan Arctic at levels approaching those of PCBs and DDTs, but the toxicological consequences are unknown. Field studies with SSL have been limited in scope and have not yet linked contaminant exposures to adverse animal health or population effects. No clear relationship between health or fitness, biomarker response and contaminant exposure has been established for SSL. Biomarkers measured in SSL and other pinnipeds include P450, immunological parameters, porphyrins and blood levels of T3, T4 and retinol. Several researchers have concluded that the utility of these biomarkers is compromised by the considerable natural variation and variable responses to contaminants. In general, biomarkers are affected by age, sex, animal condition and likely genetic variability, in addition to contaminant exposure and should be applied and interpreted with caution (Addison, 2001). Additionally, Addison (2001) and others have suggested that biomarkers should be calibrated to the extent possible and that a baseline response should be established. While biomarkers offer significant advantages in monitoring contaminant exposure and impacts because they integrate responses to complex exposures (Reinjders, 1994), additional evaluation of biomarkers applicable to SSL is needed. 11. Research recommendations Three research themes were identified by the participants at a September 2001 contaminants workshop on SSL (Barron and Heintz, 2002). Listed in general order of importance, these research themes were development of: key biolog-

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ical and ecological information for SSL (being undertaken by the Alaska Department of Fish and Game and the National Marine Mammal Laboratory); a coordinated monitoring and sample archival program; and laboratory toxicological data. An overriding data gap is that the limited contaminants data for SSL prevents rigorous statistical evaluation of contaminant trends and association between gender, age and collection location and time. Research recommendations were derived from review of contaminants workshop recommendations and ongoing research projects (Barron and Heintz, 2002), and through a comprehensive information review and evaluation. Recommended research for evaluating contaminant exposure and impacts in SSL include: (1) develop a coordinated contaminants research program and collect and report critical ancillary information on SSL (e.g. latitudeylongitude, animal condition including blubber thickness); (2) expand the sampling and analysis program to include additional chemical analytes, increased sample sizes and a broader geographic scope; (3) determine temporal and geospatial differences in contaminant exposures; (4) establish a specimen banking program; (5) determine the relative sensitivity of SSL and applicability of surrogate species benchmarks; (6) evaluate appropriate biomarkers; and (7) consider bioassay-based contaminant monitoring (e.g. H4IIE; Helm et al., 2002). Additionally, the trophic level at which juvenile SSL may feed can differ by geographic region (e.g. Ylitalo et al., 2001) and should be considered in future research. Acknowledgments We thank the numerous marine mammalogists, toxicologists and chemists that have provided information for this review, including R. Addison, K. Beckmen, P. Becker, L. Duffy, T. O’Hara, R. Norstrom, K. Pitcher and P. Ross. We also thank E. Brown for GIS support, R. Addison for reviewing the draft contaminants work plan and the participants of the 2001 SSL contaminants workshop. References Addison RF. Organochlorines and marine mammal reproduction. Can J Fish Aquat Sci 1989;46:360 –368.

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