Bioaccumulation of PCBs in Arctic seabirds: influence of dietary exposure and congener biotransformation

Four seabird species and their prey (zooplankton or fish) were collected in the Barents Sea to determine how dietary exposure, cytochrome P450 (CYP) enzyme activities and sex influenced their hepatic PCB concentrations and accumulation patterns. Five males and five females from each seabird species (little auk (Alle alle), Brunnich's guillemot (Uria lomvia), black guillemot (Cepphus grylle) and black-legged kittiwake (Rissa tridactyla)) were analysed. PCB concentrations could not be explained directly by carbon source (delta13C) or trophic position (delta15N), but by a combination of dietary parameters (delta13C, delta15N, migratory pattern, age) and contaminant metabolism. Contrary to previous studies, the PCB pattern differed among seabirds, with a higher proportion of persistent congeners (% of PCB-153, RPCB-153) in black-legged kittiwake than in auks. The PCB pattern also differed among auks, with little auk as the most efficient biotransformer (highest RPCB-153 values of persistent congeners). Based on high RPCB-153 values, Brunnich's guillemot poorly metabolised ortho-meta-unsubstituted congeners, whereas black guillemot poorly metabolised meta-para unsubstituted congeners. Species-specific differences in PCB biotransformation were confirmed by metabolic indices, where PCB patterns in seabirds were adjusted for PCB pattern in prey. The relative contribution of ortho-meta-unsubstituted congeners to SigmaPCBs decreased with increasing EROD activity. There were no differences in PCB concentrations, PCB patterns or cytochrome P450 enzyme activities between males and females. CYP P450 activities (CYP1A- and CYP2B/3A-like: EROD and testosterone 6beta-hydroxylation, respectively) were low and did not correlate with concentrations of non- or mono-ortho Cl-substituted PCBs (NO- and MO-PCBs), or with total toxic equivalent concentrations (TEQs) for dioxin-like effects of NO- and MO-PCBs.     

Comparison of organochlorine concentrations and patterns between free-ranging zooplankton and zooplankton sampled from seabirds' stomachs

To investigate the use of predators' stomach contents to measure the organochlorine load in free-ranging prey, the two zooplankton species Thysanoessa inermis (euphausiids) and Themisto libellula (amphipods) were collected simultaneously from the water column and from the seabird Brünnich's guillemot (Uria lomvia)'s stomach (from crop to proventriculus). The organochlorine compounds' concentrations and relative proportion of PCB-153 generally did not differ between the two sampling methods (least square mean of Sigma organochlorines=5.9 and 6.8 ng g(-1) wet weight for water column and stomach-sampled prey, respectively), indicating that the organochlorines in stomach-sampled prey were not yet affected by mechanical, chemical and bacterial degradation. Although the sample size is restricted, similar organochlorine concentrations and pattern in free-ranging and stomach-sampled prey may suggest that Brünnich's guillemots feed randomly on the zooplankton population rather than at more (or less) contaminated individuals. Alternatively or in addition, the similar concentrations and pattern suggest that the contaminant levels in Barents Sea zooplankton do not influence their behaviour to change the vulnerability to predation. In conclusion, the organochlorine concentrations and pattern in zooplankton collected from seabirds' stomach correspond with levels in free-ranging prey.     

Biomagnification of organochlorines along a Barents Sea food chain

To trace the biomagnification of organochlorines in marine food chains near Svalbard, which may lead to the high organochlorine concentrations in top predators from the area, we compared concentrations and patterns of organochlorines in selected taxa. The pelagic crustaceans, Calanus spp. (copepods), Thysanoessa spp. (euphausiids), Parathemisto libellula (amphipod), and the fish species, Boreogadus saida (polar cod) and Gadus morhua (cod) were selected to represent the lower trophic levels in the food web. Four seabird species were chosen at the higher trophic levels, Uria lomvia (Brünnich's guillemot), Cepphus grylle (black guillemot), Rissa tridactyla (black-legged kittiwake) and Larus hyperboreus (glaucous gull). We found low concentrations of the organochlorines sigma hexachlorocyclohexanes (sigma HCHs), hexachlorobenzene (HCB), sigma Chlordanes, sigma DDTs and sigma polychlorinated biphenyls (sigma PCBs) in crustaceans (11-50 ng g-1 lipid wt.) and fish (15-222 ng g-1 lipid wt.). In seabirds, the organochlorine concentrations biomagnified one to three orders of magnitude dependent on species and compound class. Glaucous gulls had the highest concentrations of all organochlorines. The organochlorine levels in all taxa except glaucous gull were comparable to those recorded in similar species in the Canadian Arctic. The organochlorine pattern changed from crustaceans and fish to seabirds. Moving up the food chain, the relative contribution of sigma HCHs, HCB and sigma Chlordanes decreased, and the relative contribution of sigma DDTs, sigma PCBs, persistent compounds and metabolites increased. The results reflected trophic transfer of organochlorines along the food chain as well as different elimination potentials due to direct diffusion in crustaceans and fish, and higher contaminant metabolic activity in seabirds.     

Concentrations,patterns and metabolites of organochlorine pesticides in relation to xenobiotic phase I and II enzyme activities in ringed seals (Phoca hispida) from Svalbard and the Baltic Sea

The present study investigates the concentrations and patterns of organochlorine pesticides (OCPs) and their metabolites in liver and plasma of two ringed seal populations (Phoca hispida): lower contaminated Svalbard population and more contaminated Baltic Sea population. Among OCPs, p,p′-DDE and sum-chlordanes were the highest in concentration. With increasing hepatic contaminant concentrations and activities of xenobiotic-metabolizing enzymes, the concentrations of 3-methylsulfonyl-p,p′-DDE and the concentration ratios of pentachlorophenol/hexachlorobenzene increased, and the toxaphene pattern shifted more towards persistent Parlar-26 and -50 and less towards more biodegradable Parlar-44. Relative concentrations of the chlordane metabolites, oxychlordane and -heptachlorepoxide, to sum-chlordanes were higher in the seals from Svalbard compared to the seals from the Baltic, while the trend was opposite for cis- and trans-nonachlor. The observed differences in the OCP patterns in the seals from the two populations are probably related to the catalytic activity of xenobiotic-metabolizing enzymes, and also to differences in dietary exposure.     

Organotins in marine mammals and seabirds from Norwegian territory

An increasing number of studies indicate that marine mammals and some seabirds are exposed to organotins. However, results from northern and Arctic areas are few. Here results from analysis of tributyltin (TBT), dibutyltin (DBT), monobutyltin (MBT), triphenyltin (TPhT), diphenyltin (DPhT) and monophenyltin (MPhT) in harbour porpoise (Phocoena phocoena), common seal (Phoca vitulina), ringed seal (Phoca hispida) and glaucous gull (Larus hyperboreus) from Norwegian territory are presented. Relatively high concentrations of DBT, TBT and MBT were observed in muscle, kidney and liver from harbour porpoises caught in northern Norway in 1988, just before restrictions on the use of tributyltin (TBT)(mainly on small boats) were introduced in several European countries. The concentrations in harbour porpoise muscle tissue were reduced significantly 11 years later, possibly as a result of the introduced restrictions. Considerably lower concentrations of butyltins were observed in the seals compared to porpoises. The lowest levels of organotins were found in ringed seals from Spitsbergen, where only traces of dibutyltin (DBT) and monobutyltin (MBT) were observed. Traces of DBT and MBT were also found in some individual glaucous gulls from Bear Island. The sum of the degradation products MBT and DBT in liver samples from all analysed species were generally higher than TBT itself. Triphenyltin (TPhT) was observed in all porpoise samples and in livers of common seals. Also the sum of the degradation products MPhT and DPhT in liver samples from porpoise and common seals were higher than TPhT. No traces of phenyltins were found in ringed seals from Spitsbergen or in glaucous gulls from Bear Island. The limited data available indicate low to moderate exposure to organotins in northern areas (Spitsbergen and Bear Island). Marine mammals are however more exposed further south along the Norwegian Coast.     

Flame retardants and legacy contaminants in polar bears from Alaska, Canada, East Greenland and Svalbard, 2005-2008

Flame retardants and legacy contaminants were analyzed in adipose tissue from 11 circumpolar polar bear (Ursus maritimus) subpopulations in 2005-2008 spanning Alaska east to Svalbard. Although 37 polybrominated diphenyl ethers (PBDEs), total-(α)-hexabromocyclododecane (HBCD), 2 polybrominated biphenyls (PBBs), pentabromotoluene, pentabromoethylbenzene, hexabromobenzene, 1,2-bis(2,4,6-tribromophenoxy(ethane) and decabromodiphenyl ethane were screened, only 4 PBDEs, total-(α-)HBCD and BB153 were consistently found. Geometric mean ΣPBDE (4.6-78.4 ng/g lipid weight (lw)) and BB153 (2.5-81.1 ng/g lw) levels were highest in East Greenland (43.2 and 39.2 ng/g lipid weight (lw), respectively), Svalbard (44.4 and 20.9 ng/g lw) and western (38.6 and 30.1 ng/g lw) and southern Hudson Bay (78.4 and 81.1 ng/g lw). Total-(α)-HBCD levels (<0.3-41.1 ng/g lw) were lower than ΣPBDE levels in all subpopulations except in Svalbard, consistent with greater European HBCD use versus North American pentaBDE product use. ΣPCB levels were high relative to flame retardants as well as other legacy contaminants and increased from west to east (1797-10,537 ng/g lw). ΣCHL levels were highest among legacy organochlorine pesticides and relatively spatially uniform (765-3477 ng/g lw). ΣDDT levels were relatively low and spatially variable (31.5-206 ng/g lw). However, elevated proportions of p,p'-DDT to ΣDDT in Alaska and Beaufort Sea relative to other subpopulations suggested fresh inputs from vector control use in Asia and/or Africa. Comparing earlier circumpolar polar bear studies, ΣPBDE, total-(α)-HBCD, p,p'-DDE and ΣCHL levels consistently declined, whereas levels of other legacy contaminants did not. International regulations have clearly been effective in reducing levels of several legacy contaminants in polar bears relative to historical levels. However, slow or stalling declines of certain historic pollutants like PCBs and a complex mixture of "new" chemicals continue to be of concern to polar bear health and that of their arctic marine ecosystems.     

Polychlorinated camphenes (toxaphenes), polybrominated diphenylethers and other halogenated organic pollutants in glaucous gull (Larus hyperboreus) from Svalbard and Bjørnøya (Bear Island)

The levels of polychlorinated camphenes (toxaphenes) were investigated in liver samples from 18 glaucous gulls (Larus hyperboreus) from Bj?rn?ya (74 degrees N, 19 degrees E) and four individuals from Longyearbyen (78 degrees N, 15 degrees E). Additionally brominated flame retardants (BFRs), PCBs and chlorinated pesticides were investigated in liver and intestinal contents of 15 of the glaucous gulls from Bj?rn?ya. Of the analysed BFRs only 2,2',4,4'-tetra- and 2,2',4,4',5-pentabrominated diphenylethers (PBDE 47 and 99) could be detected. The concentrations ranged between 2 and 25 ng/g ww. In addition, high resolution measurements with GC/HRMS revealed the existence of several, not quantified, PBDEs and polybrominated biphenyls (PBBs) congeners in the samples. B9-1679 and B8-1413 were the dominating toxaphenes with median concentrations of 8 and 15 ng/g ww. Concentrations of toxaphenes and PBDEs were up to 100-times lower than the concentrations of PCB and some of the pesticides. PCB and p,p/-DDE constituted 90% of the contaminants found.     

Persistent organic pollutants,heavy metals and parasites in the glaucous gull (Larus hyperboreus) on Spitsbergen

The prediction of a higher parasite infection as a consequence of an impaired immune system with increasing persistent organic pollution (POP) and heavy metal levels were investigated in adult glaucous gull (Larus hyperboreus) from Svalbard. The levels of chlorinated pesticides, polychlorinated biphenyls (PCBs), toxaphenes and polybrominated diphenyl ethers (PBDEs) were measured in liver. Cupper, cadmium, lead, mercury, selenium and zinc were measured in kidney samples. An elevated ratio of PCB-118 was found, suggesting that local contamination from the settlement was detectable in the glaucous gull. Eight cestodes, four nematodes, two acanthocephalan and three trematode helminth species were found in the intestine. A positive correlation was found between cestode intensities and selenium levels and between acanthocephalan intensities and mercury levels. No correlation was found between parasite intensities and POP concentrations. It is concluded that the contaminant levels found in glaucous gulls do not cause immune suppression severe enough to affect parasite intensity.     

Maternal transfer of organohalogen contaminants and metabolites to eggs of Arctic-breeding glaucous gulls

Eggs of seabirds have routinely been used as indicators of environmental pollution in the Arctic. However, the variability in organohalogen concentration and composition associated with the laying sequence, have not been defined. We examined a suite of PCBs, organochlorine (OC) pesticides and by-products, polybrominated diphenyl ethers (PBDEs), polybrominated biphenyls (PBBs) and methylsulfonyl- (MeSO2) PCBs in complete 3-egg clutches of glaucous gulls (Larus hyperboreus), and plasma samples of the laying females collected from the Norwegian Arctic. SigmaPCB, SigmaOC and SigmaPBDE, but not SigmaMeSO2-PCB, concentrations in eggs were positively associated, with increasing magnitude and significance from the first through the last-laid egg, with concentrations in female plasma. However, the concentrations of these organohalogen classes fluctuated irrespective of the laying order in the clutch. In general, maternal transfer favored low K(ow) and/or less persistent compounds, whereas the recalcitrant and/or higher-halogenated compounds were less readily transferred, and consequently more selectively retained in the mother.     

Organohalogen and metabolically-derived contaminants and associations with whole body constituents in Norwegian Arctic glaucous gulls

Comprehensive surveys of organohalogen contaminants have been conducted in various tissues and blood of glaucous gulls (Larus hyperboreus), a top scavenger-predator species in Svalbard in the Norwegian Arctic. However, the physico-chemical properties of organohalogens (e.g., type and degree of halogenation and the presence or absence of additional phenyl group substituents) that may influence toxicokinetics, and subsequently tissue-specific accumulation, have yet to be studied in this species. We investigated the concentrations, total body burdens, and compositional patterns of legacy chlorinated compounds (PCBs and chlordanes (CHLs)), metabolically-derived PCBs (methylsulfonyl (MeSO(2))- and OH-PCBs), brominated flame retardants (polybrominated diphenyl ethers (PBDEs), polybrominated biphenyls (PBBs), total-hexabromocyclododecane (HBCD)), and PBDE metabolites and/or naturally-occurring compounds with similar structures (MeO- and OH-PBDEs) in liver, blood and whole body homogenate samples of adult glaucous gulls (n=19) from Svalbard. Further, we examined the distribution of these organohalogens and metabolites in relation to whole body composition of glaucous gulls, i.e., the total water, protein, lipid and mineral contents in whole homogenate carcasses. The total body burden of organohalogens and metabolites in glaucous gulls ranged between 3.3 and 33.0 mg. Compound class distribution showed that the relative proportions of sum (Sigma) OH-PCB and SigmaOH-PBDE to the total organohalogen concentrations were significantly highest in blood. Conversely, the SigmaCHL and SigmaPCB showed generally higher proportions in the lipid-rich liver as well as in whole body homogenates. No significant difference in the compositional patterns of individual congeners/compounds was found among tissues/blood, with the exception of the classes comprised of less polar brominated compounds (PBDEs, PBBs and total-(alpha)-HBCD). Total proteins isolated from the whole body homogenates of glaucous gulls were significantly associated to the proportions of SigmaOH-PCB and SigmaPBDE. A non-significant positive association was found between total lipids and the SigmaPCB proportions. The present study suggests that both protein association and lipid solubility are important concomitant factors to be considered in the toxicokinetics and fate of contaminants as a function of chemical structure and properties, e.g., chlorination, bromination and the presence of other phenyl substituents such as OH group. An enhanced, selective retention of these organohalogen classes in given tissues/body compartments may thus lead to site-specific toxicological actions and adverse effects in the highly-contaminated Svalbard glaucous gulls.