Paul R. Becker

Persistent organochlorine pollutants in ringed seals and polar bears collected from northern Alaska

Blubber samples from ringed seal (Phoca hispida; n = 8) and polar bear subcutaneous fat (Ursus maritimus; n = 5) were collected near Barrow, Alaska in 1996 as part of the Alaska Marine Mammal Tissue Archival Project (AMMTAP) and retained in the National Biomonitoring Specimen Bank at the National Institute of Standards and Technology in Gaithersburg, Maryland (USA). The samples were analyzed for a variety of persistent organochlorine pollutants (POPs) including polychlorinated biphenyls (PCBs), hexachlorocyclohexanes (HCHs), chlordane and metabolites, hexachlorobenzene (HCB) and DDTs and metabolites. The geometric mean, on a wet mass basis, of sigmaPCBs (sum of 29 congeners and congener groups) were 732+/-282 ng/g (1 S.D.) in seals and 3395+/-1442 ng/g in polar bears. The geometric mean of sigmaDDTs, sigmaHCHs (alpha-, beta- and gamma- HCH) and HCB concentrations (wet mass basis) in seals and bears were 562+/-261 ng/g vs. 74.8+/-39 ng/g, 380+/-213 ng/g vs. 515 ng/g, and 17.4+/-10.1 ng/g vs. 183+/-153 ng/g, respectively. The geometric mean sum of chlordane (sigmachlordane, sum of cis- and trans-chlordane, cis- and trans-nonachlor, oxychlordane and heptachlor epoxide) and dieldrin concentrations in ringed seals and polar bears were 753+/-617 ng/g vs. 720+/-315 ng/g and 38.6+/-22.8 ng/g vs. 130+/-65 ng/g, respectively. Apparent bioaccumulation factors (polar bear/ringed seal POP concentrations) were lower in the animals sampled near Barrow, Alaska than in those from locations in the Canadian Arctic. This suggests that polar bears are also preying on marine mammals from lower trophic levels than the ringed seals with correspondingly lower organochlorine levels, such as bowhead whale carcasses. PCB congener patterns in the samples demonstrated the metabolism of certain PCB congeners in the polar bear relative to the ringed seal in agreement with previous studies. Regional comparisons of animals collected in Alaska and Arctic Canada are presented.

Review of stress in marine mammals

There has been a growing concern over the last few decades about theeffects of environmental stress, including anthropogenic impacts, onmarine mammals. This paper provides an overview of the wide range ofanthropogenic stressors that marine mammals may encounter and the levelof understanding on their potential effects. Sources of stress andphysiological responses of the animals are explored. Many of the lifehistory traits of marine mammals (i.e., long-life spans, late maturity,relatively low reproductive potential, and feeding high in the foodchain), make them susceptible to various anthropogenic stressors. Sincemarine mammals are exposed to a diverse array of multiple stressors,this paper focuses on three case studies (acute and chronic effects fromoil spills; chronic effects from environmental contaminants, andfishery-induced stress) to emphasize potential relevant hazards and toprovide a perspective on the use of marine mammals in assessingecosystem health. Additional research to enhance our understanding ofstress on marine mammals and to provide the science needed to guidemanagement decisions is recommended.

Organochlorine contaminants in blubber of four seal species: Integrating biomonitoring and specimen banking

Blubber samples from four Alaska seal species (bearded seal, Erignathus barbatus, harbor seal, Phoca vitulina, northern fur seal, Callorhinus ursinus, ringed seal, P. hispida) were collected for inclusion in the US National Biomonitoring Specimen Bank, as well as for immediate analysis as part of the contaminant monitoring component of the US National Marine Fisheries Services Marine Mammal Health and Stranding Response Program. The blubber samples were analyzed for organochlorine (OC) contaminants (e.g., PCB congeners, pesticides, DDTs). Results for bearded and ringed seals from the Alaska Arctic revealed low blubber concentrations of OC contaminants. Harbor seals from Prince William Sound. Gulf of Alaska, had somewhat higher blubber concentrations of OC contaminants. In contrast, northern fur seals sampled from the Pribilof Islands had blubber concentrations of certain OC contaminants that were about an order of magnitude higher than those found in the other seal species. Differences in contaminant concentrations among the Alaska seals may be explained by differences in feeding habits and migratory patterns, age or gender did not appear to account for the differences observed. The highest concentrations of OCs were found in harbor seals stranded along the northwestern US mainland, which is consistent with higher concentrations of anthropogenic contaminants being found in urban coastal areas than in more remote Arctic environments. The integration of real-time contaminant monitoring with specimen banking provides important baseline data that can be used to plan and manage banking activities. This includes identifying appropriate specimens that are useful in assessing temporal trends and increasing the utility of the banked samples in assessing chemical contaminant accumulation and relationships to biological effects.

Determination of arsenic compounds in marine mammals with high-performance liquid chromatography and an inductively coupled plasma mass spectrometer as element-specific detector

Total arsenic concentrations and the concentrations of individual arsenic compounds were determined in liver samples of pinnipeds [nine ringed seals (Phoca hispida), one bearded seal (Erginathus barbatus)] and cetaceans [two pilot whales (Globicephalus melas), one beluga whale (Deliphinapterus leucus)]. Total arsenic concentrations ranged from 0.167 to 2.40 mg As kg -1 wet mass. The arsenic compounds extracted from the liver samples with a methanol/water mixture (9:1, v/v) were identified and quantified by anion- and cation-exchange chromatography. An ICP-MS equipped with a hydraulic highpressure nebulizer served as the arsenic-specific detector. Arsenobetaine (0.052-1.67 mg As kg -1 wet mass) was the predominant arsenic compound in all the liver samples. Arsenocholine was present in all livers (0.005-0.044 mg As kg -1 wet mass). The tetramethylarsonium cation was detected in all pinnipeds (<0.009 to 0.043 mg Askg -1 ) but not in any of the cetaceans. The concentration of dimethylarsinic acid ranged from < 0.001 to 0.109mgAskg -1 wet mass. Most of the concentrations for methylarsonic acid (<0.001 to 0.025 mg As kg -1 wet mass) were below the detection limit. Arsenous acid and arsenic acid concentrations were below the detection limit of the method (0.001 mg As kg -1 ). An unknown arsenic compound was present in all liver samples at concentrations from 0.002-0.027 mg As kg -1 .

ORGANOCHLORINE CONTAMINANT LEVELS IN ESKIMO HARVESTED BOWHEAD WHALES OF ARCTIC ALASKA

Organochlorine (OC) levels in liver and blubber of 20 bowhead whales (Balaena mysticetus) collected during the Eskimo subsistence harvest at Barrow (Alaska, USA) in 1992 and 1993 are presented. Liver sum DDT (lipid weight) was significantly greater in male whales than in females. Most of the organochlorines measured were at higher levels in longer (older) than in shorter (younger) males. For female bowhead whales, hexachlorobenzene and lipid levels decreased and other OC levels did not change significantly with increasing length. Most organo-chlorine contaminants have low concentrations in tissues of the bowhead whale compared to concentrations in tissues of other cetaceans, especially Odontocetes. Based on allowable daily intakes (ADI) levels established by the Canadian Northern Contaminants Program (Ottawa, Ontario, Canada) “safe” levels of blubber to consume were calculated. Chlordane levels in bowhead whale blubber results in the most restrictive consumption amount (50 g blubber/day). We expect no adverse effects related to these organochlorine contaminants to occur in bowhead whales or in consumers of their tissues. However, investigation of low level chronic exposure effects and a more rigorous assessment of histopathology, biomarkers, and immune status in the bowhead whale would be required to conclude “no effect” with more certainty.

Concentrations of chlorinated hydrocarbons and trace elements in marine mammal tissues archived in the U.S. national biomonitoring specimen bank

The U.S. National Biomonitoring Specimen Bank (NBSB) provides for the long term storage of well documented and preserved specimens representing several types of environmental matrices. A major part of this inventory consists of marine mammal tissues (e.g., blubber, liver, kidney, and muscle). Within the NBSB selected specimens are periodically analyzed for chlorinated hydrocarbons and trace elements. Although only 20% of the 560 marine mammal specimens in the NBSB have been analyzed, the database is of value in evaluating the stability of analytes and sample degradation during storage, for comparing with results from samples collected in the future for long-term monitoring, and for comparing with analytical results from other laboratories on samples collected at the same time for monitoring purposes. The NBSB analytical database contains results for 37 elements, many of which are not analyzed routinely by conventional analytical techniques used in monitoring programs, and the following organic compounds: selected PCB congeners. DDT compounds, alpha- and gamma-HCH, HCB, heptachlor epoxide, oxychlordane, cis-chlordane, trans-chlordane, cis-nonachlor, trans-nonachlor, and dieldrin in 9 marine mammal species: northern fur seal (Callorhinus ursinus), ringed seal (Phoca hispida), spotted seal (P. largha), bearded seal (Erignathus barbatus), pilot whale (Globicephala melas), harbor porpoise (Phocoena phocoena), white-sided dolphin (Lagenorhynchus acutus), beluga whale (Delphinapterus leucas), and bowhead whale (Balaena mysticetus). Analyses of beluga whale blubber for toxaphene and additional chlorinated hydrocarbons are obtained through collaboration with the Department of Fisheries and Oceans Canada.

Spatial and temporal trends of perfluorinated compounds in Beluga Whales (Delphinapterus leucas) from Alaska.

Wildlife from remote locations have been shown to bioaccumulate perfluorinated compounds (PFCs) in their tissues. Twelve PFCs, consisting of perfluorinated carboxylic (PFCA) and sulfonic (PFSA) acids as well as the perfluorooctane sulfonate (PFOS) precursor perfluorooctane sulfonamide (PFOSA), were measured in livers of 68 beluga whales (Delphinapterus leucas) collected from two subpopulations, Cook Inlet and eastern Chukchi Sea, in Alaska between 1989 and 2006. PFOS and PFOSA were the dominant compounds measured in both beluga stock populations, with overall median concentrations of 10.8 ng/g and 22.8 ng/g, respectively. Long-chain perfluorocarboxylates, PFCAs (9 to 14 carbons), were detected in more than 80% of the samples. Perfluoroundecanoic acid (PFUnA) and perfluorotridecanoic acid (PFTriA) made up a large percentage of the PFCAs measured with median concentrations of 8.49 ng/g and 4.38 ng/g, respectively. To compare differences in location, year, sex, and length, backward stepwise multiple regression models of the individual and total PFC concentrations were used. Spatially, the Cook Inlet belugas had higher concentrations of most PFCAs and PFOS (p < 0.05); however, these belugas had a lower median concentration of PFOSA when compared to belugas from the eastern Chukchi Sea (p < 0.05). Temporal trends indicated most PFCAs, PFHxS, PFOS, and PFOSA concentrations increased from 1989 to 2006 (p < 0.05). Males had significantly higher concentrations of PFTriA, ΣPFCA, and PFOS (p < 0.05). Perfluorononanic acid (PFNA) and PFOS showed a significant decrease in concentration with increasing animal length (p < 0.05). These observations suggest the accumulation of PFCs in belugas is influenced by year, location, sex, and length.

Concentration of Chlorinated Hydrocarbons and Heavy Metals in Alaska Arctic Marine Mammals

Over the last decade, a baseline database on anthropogenic contaminants in Alaska marine mammals has been developing through the efforts of several independent investigations as well as larger research programs. Although still somewhat limited in scope, the largest amount of data exists for polychlorinated biphenyls (PCBs), DDT, mercury, and cadmium in walrus, beluga whale, bowhead whale, and ringed seal. Because of their relatively large contribution to the total chlorinated hydrocarbon levels in Arctic species, chlordane and toxaphene are two pesticides that are also gaining attention. Comparison of the Alaska database with the results of studies conducted in Canada and Greenland, indicates that patterns of many accumulative substances are quite similar in species that occur across the North American Arctic.

Spatial and temporal trends of persistent organic pollutants and mercury in beluga whales (Delphinapterus leucas) from Alaska.

Remote locations, such as the Arctic, are often sinks for persistent contaminants which can ultimately bioaccumulate in local wildlife. Assessing temporal contaminant trends in the Arctic is important in understanding whether restrictions on legacy persistent organic pollutants (POPs) have led to concentration declines. Beluga whale (Delphinapterus leucas) tissue samples were collected from two subpopulations (Cook Inlet, Alaska and the eastern Chukchi Sea) between 1989 and 2006. Several POPs (polychlorinated biphenyls (PCBs), dichlorodiphenyldichloroethane and related compounds (DDTs), chlordanes, hexachlorocyclohexanes (HCHs), chlorobenzenes, mirex, polybrominated diphenyl ethers (PBDEs) and semi-quantitatively hexabromocyclododecanes (HBCDs)) were measured in 70 blubber samples, and total mercury (Hg) was measured in 67 liver samples from a similar set of individuals. Legacy POPs (PCBs, chlordanes, DDTs, and HCHs) were the predominant organic compound classes in both subpopulations, with median concentrations of 2360ng/g lipid for Σ80PCBs and 1890 ng/g lipid for Σ6DDTs. Backward stepwise multiple regressions showed that at least one of the four independent variables (subpopulation, sampling year, sex, and animal length) influenced the POP and Hg concentrations. ΣPCBs, ΣDDTs, Σchlordanes, Σchlorobenzenes, mirex, and Hg were significantly higher in belugas from the eastern Chukchi Sea than from the Cook Inlet (p≤0.0001). In contrast, Σ8PBDE and α-HBCD concentrations were significantly lower in belugas from the eastern Chukchi Sea than from the Cook Inlet (p<0.0001). Significant temporal increases in concentrations of Σ8PBDE and α-HBCD were observed for both subpopulations (p≤0.0003), and temporal declines were seen for ΣHCHs and Σchlorobenzenes in eastern Chukchi Sea belugas only (p≤0.0107). All other POP and Hg concentrations were stable, indicating either a lagging response of the Arctic to source reductions or the maintenance of concentrations by unregulated sources. Sex and length also significantly influenced some concentrations, and these findings are discussed.

Factors influencing persistent organic pollutant concentrations in the Atlantic white-sided dolphin (Lagenorhynchus acutus).

Assessing the trends of persistent organic pollutants (POPs) in cetaceans is difficult because of age and gender influences on accumulation. Persistent organic pollutants bioaccumulate and are poorly metabolized; hence, concentrations may increase with age in males while females reduce their POP burden through parturition and lactation. Age and gender effects on contaminant concentrations are species specific because of life history and reproductive strategies. These influences must be understood in order to elucidate and assess lifetime POP exposure. The objectives of this study were to determine baseline POP concentrations in blubber samples from the Atlantic white-sided dolphin (Lagenorhynchus acutus) and to investigate life history and other influences, such as metabolism, on these concentrations. Forty-seven L. acutus blubber samples collected from mass stranding events in Massachusetts, USA (1993-2000), and archived in the National Marine Mammal Tissue Bank at the National Institute of Standards and Technology (Gaithersburg, MD, USA) were analyzed for 55 polychlorinated biphenyl congeners (PCB; 55 congeners), five polybrominated diphenyl ether (PBDE) congeners, and organochlorine pesticides (toxaphene, DDT and metabolites, mirex, dieldrin, chlordanes, hexachlorocyclohexanes, hexachlorobenzene, and endosulfans) by gas chromatography/mass spectrometry (GC-MS). Ages for 19 animals were determined from growth layer groups on decalcified, stained thin tooth sections. Total PCBs (sigmaPCB; sum of 55 congeners) were the contaminants present in the highest concentrations in all age classes (0.5-63 microg/g wet mass) followed by sum of DDTs (0.50-43 microg/g wet mass), toxaphene (0.055-31 microg/g wet mass), chlordanes (0.30-24 microg/g wet mass), and PBDEs (0.12-4.0 microg/g wet mass). Body length had a greater statistical influence than age on contaminant burdens in L. acutus. Contaminant burdens decreased with length in both male and female L. acutus, suggesting metabolic elimination and/or growth dilution in males and off-loading via lactation in females.