Liesbeth Weijs

Inter-species differences for polychlorinated biphenyls and polybrominated diphenyl ethers in marine top predators from the Southern north Sea: Part 1. Accumulation patterns in harbour seals and harbour porpoises

Harbour porpoises (Phocoena phocoena) and harbour seals (Phoca vitulina) are two representative top predator species of the North Sea ecosystem. The median values of sum of 21 polychlorinated biphenyl (PCB) congeners and sum of 10 polybrominated diphenyl ether (PBDE) congeners were 23.1 microg/g lipid weight (lw) and 0.33 microg/g lw in blubber of harbour seals (n=28) and 12.4 microg/g lw and 0.76 microg/g lw in blubber of harbour porpoises (n=35), respectively. For both species, the highest PCB concentrations were observed in adult males indicating bioaccumulation. On the contrary, the highest PBDE concentrations were measured in juveniles, likely due to better-developed metabolic capacities with age in adults. A higher contribution of lower chlorinated and non-persistent congeners, such as CB 52, CB 95, CB 101, and CB 149, together with higher contributions of other PBDE congeners than BDE 47, indicated that harbour porpoises are unable to metabolize these compounds. Harbour seals showed a higher ability to metabolize PCBs and PBDEs.

Anthropogenic and naturally-produced organobrominated compounds in marine mammals from Brazil

Liver samples from 51 cetaceans, comprising 10 species, stranded between 1994 and 2006 in a highly industrialized and urbanized region in Southeast Brazil, were analyzed for polybrominated diphenyl ethers (PBDEs) and methoxylated-PBDEs (MeO-PBDEs). A concentration range of PBDEs (3-5960ng/g lw) similar to that observed in Northern Hemisphere dolphins was found. MeO-PBDE concentrations in continental shelf (CS) dolphins from Brazil are among the highest detected to date in cetaceans (up to 250microg/g lw). Higher SigmaMeO-PBDE concentrations were measured in CS and oceanic dolphins than in estuarine dolphins. The SigmaPBDE/SigmaMeO-PBDE ratio varied significantly ranging from a mean value of 7.12 to 0.08 and 0.01 for estuarine, CS and oceanic species, respectively. A positive correlation was observed between SigmaPBDE and year of stranding of male estuarine dolphins (Sotalia guianensis), which suggests temporal variation in the exposure. Placental transfer of organobrominated compounds was also evidenced in S. guianensis.

Concentrations of chlorinated and brominated contaminants and their metabolites in serum of harbour seals and harbour porpoises

Harbour seals (Phoca vitulina) and harbour porpoises (Phocoena phocoena) are top predators in the North Sea and consequently accumulate a variety of pollutants in their tissues. Concentrations of polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and their hydroxylated metabolites (HO-PCBs and HO-PBDEs) were measured in serum of wild harbour seals (n=47) and captive harbour porpoises (n=21). Both species exhibit long life spans and do not have extreme situations, such as complete fasting during periods of lactation, in their annual cycles. For PCBs, concentrations in adult males were slightly higher than in juveniles and lowest in juvenile females. For PBDEs, juveniles have higher levels than adult males and females, probably as a consequence of lactational transfer. However, differences between these age-gender groups were not statistical significant, indicating that individual variation was limited within each species, even without knowing the feeding status of the animals. Body condition, particularly emaciation, has a major influence on the levels of chlorinated and brominated contaminants in serum. Profiles of PCBs were CB 153>CB 138>CB 187>CB 180 and CB 153>CB 138>CB 149>CB 187>CB 180 for harbour seals and porpoises respectively. For PBDEs, BDE 47 was the predominant congener followed by BDE 100 and 99 in both species. In harbour seals, concentrations of sum PCBs (median: 39,200 pg/ml) were more than 200 times higher than levels of sum PBDEs (median: 130 pg/ml) and almost 10 times higher than concentrations of sum HO-PCBs (4350 pg/ml). In harbour porpoises, concentrations of sum PCBs (median: 24,300 pg/ml) were about 20 times higher than concentrations of PBDEs (median: 1300 pg/ml). HO-PCBs were detected in only 4 harbour porpoises and this at very low concentrations. Naturally-produced MeO-PBDEs were only found in harbour porpoises at concentrations ranging from 120 to 810 pg/ml. HO-PBDEs were not found in any species. In general, harbour seals accumulate less compounds and have mostly lower concentrations than harbour porpoises possibly as a result of a better developed metabolism.

Tissue-specific accumulation of polybrominated diphenyl ethers (PBDEs) including Deca-BDE and hexabromocyclododecanes (HBCDs) in harbor seals from the northwest Atlantic

Polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecanes (HBCDs) are widely used flame retardants that enter coastal waters from multiple sources and biomagnify in marine food webs. PBDEs have been detected at relatively high concentrations in harbor seals, apex predators in the northwest Atlantic. Whereas tri- to hexa-BDEs readily biomagnified from prey fishes to seal blubber, Deca-BDE (BDE-209) did not biomagnify in blubber. To explore tissue-specific differences in the accumulation/biomagnification of BFRs, we analyzed tri- to Deca-BDES in liver of 56 harbor seals (6 adult males, 50 pups), and compared hepatic concentrations and biomagnification potential with those in blubber. HBCDs were analyzed in seal liver and blubber to enable similar comparisons. Hepatic ΣPBDE (tri- to Octa-BDE) concentrations (range 35-19,547ng/glipid weight, lw) were similar to blubber concentrations, while α-HBCD levels in seal liver (range 2-279ng/glw) were significantly higher than levels in blubber. Tissue distribution of PBDEs and α-HBCD varied significantly by age and, surprisingly, by gender among the pups. Biomagnification of α-HBCD from fish to seal liver and blubber was negligible to low, implying that harbor seals can metabolize this persistent isomer. Similar to the patterns in blubber, tri- through hexa-BDEs were highly biomagnified from fish to seal liver. In contrast, BDE-209 concentrations in liver were up to five times higher than those in blubber, which is consistent with observations that BDE-209 migrates to perfused tissues such as the liver in biota. Although detection frequency was low, BDE-209 levels in seal liver were up to ten times higher than those in their prey fish, suggesting that the accumulation/biomagnification of Deca-BDE in marine food webs is tissue-specific. As BDE-209 is the dominant PBDE found in marine sediments, its biomagnification in marine ecosystems is of concern.

Selective transfer of persistent organic pollutants and their metabolites in grey seals during lactation.

Twenty grey seal (Halichoerus grypus) mother-pup pairs from the colony of the Isle of May (Scotland) were sampled at early and late lactation in order to study the transfer of polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and their metabolites (HO-PCBs and HO-PBDEs) as well as organochlorine pesticides (OCPs), such as DDT and metabolites (DDXs) and hexachlorobenzene (HCB). The transfer of the naturally produced MeO-PBDEs was also investigated. Generally, concentrations (on a lipid weight basis) of the sum of PCBs, PBDEs and DDXs tended to be higher in all tissues at late lactation (for maternal outer blubber ΣPCBs=3860±2091 ng/g, ΣPBDEs=120±74 ng/g and ΣDDXs=559±207 ng/g; for maternal inner blubber ΣPCBs=4229±3274 ng/g, ΣPBDEs=148±118 ng/g and ΣDDXs=704±353 ng/g; for maternal serum ΣPCBs=1271±796 ng/g, ΣPBDEs=27±16 ng/g and ΣDDXs=242±125 ng/g; for milk ΣPCBs=1190±747 ng/g, ΣPBDEs=55±36 ng/g and ΣDDXs=357±160 ng/g; for pup serum ΣPCBs=1451±901 ng/g, ΣPBDEs=48±31 ng/g and ΣDDXs=395±201 ng/g). In all tissues, ΣMeO-PBDEs were found at very low levels or even undetected and their concentrations appeared to increase at late lactation only in maternal inner blubber (2.7±1.3 to 5.3±2.9 ng/g for early and late lactation, respectively) and milk (0.6±0.3 to 1.1±0.5 ng/g for early and late lactation, respectively). The transfer from inner blubber to maternal serum was selective and strongly depended on the log K(ow) value of the compounds, with less lipophilic compounds being more efficiently released. Only a limited amount of HO-PCBs was transferred during lactation as 4-HO-CB-107 was the only metabolite detected in milk (29 to 40 pg/g lw). On the contrary, most of HO-PCB metabolites found in maternal serum were also detected in pup serum. These findings suggest not only a transplacental transfer of HO-PCBs from mothers to pups but also the possibility of endogenous biotransformation in suckling pups or accumulation of undetectable low amounts from milk.

Occurrence of anthropogenic and naturally-produced organohalogenated compounds in tissues of Black Sea harbour porpoises.

Harbour porpoises are one of the three cetacean species inhabiting the Black Sea. This is the first study to report on polybrominated diphenyl ethers (PBDEs) and naturally-produced compounds, methoxylated PBDEs (MeO-PBDEs) and polybrominated hexahydroxanthene derivatives (PBHDs), in tissues (kidney, brain, blubber, liver, muscle) of male harbour porpoises (11 adults, 9 juveniles) from the Black Sea. Lipid-normalized concentrations decreased from muscle>blubber>liver>kidney>brain for the sum of polychlorinated biphenyls (PCBs) and for the sum of PBDEs. Among the naturally-produced compounds, levels of PBHDs were higher than of MeO-PBDEs, with tri-BHD and 6-MeO-BDE 47 being the dominant compounds for both groups, respectively. Concentrations of naturally-produced compounds decreased from blubber to brain, similarly to the sum of DDT and metabolites (DDXs). Concentrations of DDXs were highest, followed by PCBs, HCB, PBHDs, PBDEs and MeO-PBDEs. Levels of PCBs and PBDEs in blubber were lower than concentrations reported for harbour porpoises from the North Sea, while concentrations of DDXs were higher.

Persistent organic pollutants and methoxylated PBDEs in harbour porpoises from the North Sea from 1990 until 2008: Young wildlife at risk?

In the European North Sea, harbour porpoises are top predators with relatively long life spans and a limited capacity for metabolic biotransformation of contaminants compared to some other marine mammal species. As such, they are exposed to a mixture of persistent pollutants, such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), DDT and metabolites (DDXs), hexachlorobenzene (HCB) and chlordanes (CHLs) that bioaccumulate in their tissues. We report here on the levels of persistent organic pollutants and of the naturally-produced methoxylated PBDEs (MeO-PBDEs) in blubber, liver and kidney of harbour porpoise neonates (n=3), calves (n=15), juveniles (n=6) and adults (n=4) of the southern North Sea. Concentrations of almost all contaminant classes decrease slightly in all age groups over the period 1990-2008. For some classes (e.g. PCBs and DDXs) however, levels seem to increase little in harbour porpoise calves. In all animals, blubber had the highest concentrations, followed by liver and kidney, whereas liver and kidney were the preferred tissues for several compounds, such as octa- and deca-PCBs. Our data suggest that harbour porpoises calves are exposed to higher or comparable concentrations of POPs and of MeO-PBDEs and somewhat different patterns of selected POPs than adults, potentially placing them, and the entire population, at a disproportionate risk for exposure-related health effects.

ANTHROPOGENIC AND NATURALLY-PRODUCED ORGANOBROMINATED COMPOUNDS IN BLUEFIN TUNA FROM THE MEDITERRANEAN SEA

Anthropogenic compounds, such as polybrominated diphenyl ethers (PBDEs), together with naturally-produced organobromines, such as methoxylated PBDEs (MeO-PBDEs), polybrominated hexahydroxanthene derivatives (PBHDs), 2,4,6-tribromoanisole (TBA) and a mixed halogenated monoterpene (MHC-1), were measured in muscle from 26 farmed and wild bluefin tuna (Thunnus thynnus) caught in the Mediterranean Sea. This species is ecological attractive because of the changes of geographic habitat throughout its long lifespan which affect its feeding. PBDE concentrations were similar between tuna samples of different groups (17-149 ng g(-1) lipid weight - lw in farmed tuna, 25-219 ng g(-1)lw in longline fished tuna and 26-126 ng g(-1)lw in net-fished tuna). However, higher concentrations of naturally-produced MeO-PBDEs and PBHDs were observed in the two types of wild tuna (longline fished and net-fished) compared to farmed tuna suggesting that wild tunas come easily in contact with sources of these compounds. In all cases PBHDs presented the highest contribution to the sum of organobromines (50% in farmed tuna and >90% in wild tuna). TBA was detected at low concentrations (<6 ng g(-1)lw), while MHC-1 was found at higher concentrations (up to 42 ng g(-1)lw) in farmed tuna. The estimated daily ingestion of PBDEs from tuna was 830 ng PBDEs day(-1), regardless of the origin of the tuna. While this value is approximately 600 times lower than the minimum risk level set by the US Department of Health and Human Services, it is approximately eight times higher than the total intake of PBDEs via diet, suggesting that consumption of tuna can add considerably to the total daily intake of PBDEs.

Physiologically Based Pharmacokinetic (PBPK) Models for Lifetime Exposure to PCB 153 in Male and Female Harbor Porpoises (Phocoena phocoena): Model Development and Evaluation

Physiologically based pharmacokinetic (PBPK) models were developed for the most persistent polychlorinated biphenyl (PCB 153) in male and female harbor porpoises (Phocoena phocoena) to elucidate processes such as uptake, distribution, and elimination. Due to its limited metabolic capacities, long life span, and top position in marine food chains, this species is highly sensitive to pollution. The models consist of 5 compartments, liver, blubber, kidney, brain, and a compartment which accounts for the rest of the body, all connected through blood. All physiological and biochemical parameters were extracted from the literature, except for the brain/blood partition coefficient and rate of excretion, which were both fitted to data sets used for validation of the models. These data sets were compiled from our own analyses performed with GC-MS on tissue samples of harbor porpoises. The intake of PCB 153 was from milk from birth to 4 months, and after weaning fish was the main food source. Overall, these models reveal that concentrations of PCB 153 in males increase with age but suggest that, as the animals grow older, metabolic transformation can be a possible pathway for elimination as well. In contrast, the model for females confirms that gestation and lactation are key processes for eliminating PCB 153 as body burdens decrease with age. These PBPK models are capable of simulating the bioaccumulation of PCB 153 during the entire life span of approximately 20 years of the harbor porpoises.

Assessing levels of halogenated organic compounds in mass-stranded long-finned pilot whales (Globicephala melas) from Australia

Pollution is a threat to the health of marine mammals worldwide. Mass-strandings are poorly understood, but often involve pilot whales. However, there is limited information regarding pollution in long-finned pilot whales from Australia. Consequently, the profiles and levels of several pollutant classes were investigated in blubber of Tasmanian long-finned pilot whales. DDX levels were highest in all groups, followed by PCBs or MeO-PBDEs and lowest for PBDEs. The concentrations of all pollutants decreased with age in males. This is at least partly due to the growth dilution effect although it might also be caused by decreasing levels of PCBs, PBDEs, DDXs, HCB and CHLs in the environment. Fetus/mother ratios of higher chlorinated PCBs increased with the duration of pregnancy suggesting a preference for offloading via gestation rather than through lactation. Overall, the highest pollutant levels were found in the youngest animals.