Veerle L.B. Jaspers

Brominated flame retardants and organochlorines in the European environment using great tit eggs as a biomonitoring tool

Large-scale studies are essential to assess the emission patterns and spatial distribution of organohalogenated pollutants (OHPs) in the environment. Bird eggs have several advantages compared to other environmental media which have previously been used to map the distribution of OHPs. In this study, large-scale geographical variation in the occurrence of OHPs, such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and organochlorine pesticides (OCPs), was investigated throughout Europe using eggs of a terrestrial residential passerine species, the great tit (Parus major). Great tit eggs from 22 sampling sites, involving urban, rural and remote areas, in 14 European countries were collected and analysed (5-8 eggs per sampling site). The environmentally most important congeners/compounds of the analysed pollutants were detectable in all sampling locations. For PCBs, PBDEs and OCPs, no clear geographical contamination pattern was found. Sum PCB levels ranged from 143 ng/g lipid weight (lw) to 3660 ng/g lw. As expected, PCB concentrations were significantly higher in the sampled urban compared to the remote locations. However, the urban locations did not show significantly higher concentrations compared to the rural locations. Sum PBDEs ranged from 4.0 ng/g lw to 136 ng/g lw. PBDEs were significantly higher in the urbanized sampling locations compared to the other locations. The significant, positive correlation between PCB and PBDE concentrations suggests similar spatial exposure and/or mechanisms of accumulation. Significantly higher levels of OCPs (sum OCPs ranging from 191 ng/g lw to 7830 ng/g lw) were detected in rural sampling locations. Contamination profiles of PCBs, PBDEs and OCPs differed also among the sampling locations, which may be due to local usage and contamination sources. The higher variance among sampling locations for the PCBs and OCPs, suggests that local contamination sources are more important for the PCBs and OCPs compared to the PBDEs. To our knowledge, this is the first study in which bird eggs were used as a monitoring tool for OHPs on such a large geographical scale.

Can predatory bird feathers be used as a non-destructive biomonitoring tool of organic pollutants?

The monitoring of different types of pollutants that are released into the environment and that present risks for both humans and wildlife has become increasingly important. In this study, we examined whether feathers of predatory birds can be used as a non-destructive biomonitor of organic pollutants. We demonstrate that polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDT) and polybrominated diphenyl ethers (PBDEs) are measurable in one single tail feather of common buzzards (Buteo buteo) and that levels in this feather and internal tissues are significantly related to each other (0.35<r<0.76 for all 43 buzzards; 0.46<r<0.84 when excluding 17 starved birds). Our findings provide the first indication that feathers of predatory birds could be useful in non-destructive biomonitoring of organic pollutants, although further validation may be necessary.

An overview of existing raptor contaminant monitoring activities in Europe

Biomonitoring using raptors as sentinels can provide early warning of the potential impacts of contaminants on humans and the environment and also a means of tracking the success of associated mitigation measures. Examples include detection of heavy metal-induced immune system impairment, PCB-induced altered reproductive impacts, and toxicity associated with lead in shot game. Authorisation of such releases and implementation of mitigation is now increasingly delivered through EU-wide directives but there is little established pan-European monitoring to quantify outcomes. We investigated the potential for EU-wide coordinated contaminant monitoring using raptors as sentinels. We did this using a questionnaire to ascertain the current scale of national activity across 44 European countries. According to this survey, there have been 52 different contaminant monitoring schemes with raptors over the last 50years. There were active schemes in 15 (predominantly western European) countries and 23 schemes have been running for >20years; most monitoring was conducted for >5years. Legacy persistent organic compounds (specifically organochlorine insecticides and PCBs), and metals/metalloids were monitored in most of the 15 countries. Fungicides, flame retardants and anticoagulant rodenticides were also relatively frequently monitored (each in at least 6 countries). Common buzzard (Buteo buteo), common kestrel (Falco tinnunculus), golden eagle (Aquila chrysaetos), white-tailed sea eagle (Haliaeetus albicilla), peregrine falcon (Falco peregrinus), tawny owl (Strix aluco) and barn owl (Tyto alba) were most commonly monitored (each in 6-10 countries). Feathers and eggs were most widely analysed although many schemes also analysed body tissues. Our study reveals an existing capability across multiple European countries for contaminant monitoring using raptors. However, coordination between existing schemes and expansion of monitoring into Eastern Europe is needed. This would enable assessment of the appropriateness of the EU-regulation of substances that are hazardous to humans and the environment, the effectiveness of EU level mitigation policies, and identify pan-European spatial and temporal trends in current and emerging contaminants of concern.

An exposure study with polybrominated diphenyl ethers (PBDEs) in female European starlings (Sturnus vulgaris): Toxicokinetics and reproductive effects

We exposed female European starlings to a pentabromodiphenyl ether (Penta-BDE) mixture through subcutaneous implants, and examined levels and profiles of polybrominated diphenyl ethers (PBDEs) together with reproductive effects. Sum PBDE levels increased significantly in the serum of the exposed females from 218+/-43 to 23,400+/-2035 pg/ml. Sum PBDE concentrations in the eggs of the exposed group ranged from 130+/-12 to 220+/-37 ng/g wet weight (ww). The profile in serum after egg laying was very similar to that in eggs. There were no detectable levels of HO-PBDEs in both serum and eggs. Fewer females of the exposed group initiated egg laying compared to the control group, although the difference was not significant. In addition, egg weight and volume were significantly higher in the exposed group. These results suggest that, at the investigated exposure levels (150 microg sum PBDEs/bird), PBDEs may have a negative effect on reproductive performance.

A first evaluation of the usefulness of feathers of nestling predatory birds for non-destructive biomonitoring of persistent organic pollutants

In previous studies, feathers of adult predatory birds have been evaluated as valid non-destructive biomonitor matrices for persistent organic pollutants (POPs). In this study, we assessed for the first time the usefulness of nestling raptor feathers for non-destructive biomonitoring of POPs. For this purpose, we collected body feathers and blood of nestlings from three avian top predators from northern Norway: northern goshawks (Accipiter gentilis), white-tailed eagles (Haliaeetus albicilla) and golden eagles (Aquila chrysaetos). We were able to detect a broad spectrum of legacy POPs in the nestling feathers of all three species (Σ PCBs: 6.78-140ng g(-1); DDE: 3.15-145ng g(-1); Σ PBDEs: 0.538-7.56ng g(-1)). However, these concentrations were lower compared to other studies on raptor species, probably due to the aspect of monitoring of nestlings instead of adults. Besides their analytical suitability, nestling feathers also appear to be biologically informative: concentrations of most POPs in nestling feathers showed strong and significant correlations with blood plasma concentrations in all species (p<0.050; 0.775<r<0.994). In addition, the reported correlations between feathers and blood plasma were much higher than those previously reported for adult individuals. Accumulation profiles and species-specific differences were in accordance with other toxicological studies on avian species and generally in agreement with the specific ecology of the studied species. In summary, our results indicate that the use of nestling feathers of northern raptors may be a valid and promising non-destructive biomonitoring strategy for POPs in their ecosystems.

The relationship between perfluorinated chemical levels in the feathers and livers of birds from different trophic levels.

Although feathers have been used successfully for monitoring heavy metals and organic pollutants, there are currently no data available on the use of feathers as indicators of perfluorinated chemical (PFC) exposure in birds. Also, no study has evaluated PFC levels in birds with different diets from different habitats. In the current study we investigated the PFC exposure of five different bird species from the same geographic region in Belgium, using both feathers and liver tissue. The highest mean liver perfluorooctane sulfonate (PFOS) levels were found in the Grey Heron (476 ng/g ww) followed by the Herring Gull (292 ng/g ww) and Eurasian Sparrowhawk (236 ng/g ww), whereas the Eurasian Magpie (17 ng/g ww) and the Eurasian Collared Dove (12 ng/g ww) had the lowest levels. The PFOS levels in the feathers showed a different pattern. The Grey Heron had the highest feather PFOS levels (247 ng/g dw), the Eurasian Sparrowhawk (102 ng/g dw) had the second highest feather PFOS levels, followed by the Herring Gull (79 ng/g dw) and the Eurasian Collared Dove (48 ng/g dw), and the lowest levels were found in the Eurasian Magpie (31 ng/g dw). Overall, there was a significant positive correlation (Pearson, R=0.622, p<0.01) between the feather and liver PFOS levels, indicating that feathers could be an alternative bioindicator for PFOS exposure in birds. However, caution should be taken as there was no significant correlation between the PFOS levels in the feathers and livers of the individual species. In general, birds from a higher trophic level had higher PFC levels in their tissues. This indicates that diet plays a role in PFC exposure in birds and confirms the bioaccumulation potential of PFC.

Relationships between organohalogen contaminants and blood plasma clinical–chemical parameters in chicks of three raptor species from Northern Norway

Organohalogen contaminants (OHCs) may affect various physiological parameters in birds including blood chemistry. We therefore examined blood plasma clinical-chemical parameters and OHCs in golden eagle, white-tailed eagle and goshawk chicks from Northern Norway. Correlation analyses on pooled data showed that alkaline phosphatase (ALKP), glucose and creatinine were significantly negatively correlated to various OHCs (all: p<0.05; r: -0.43 to -0.55; n=23), while alanine aminotransferase (ALAT), total protein, cholesterol, uric acid, total bilirubin, ratios protein:creatinine and uric acid:creatinine were significantly positively correlated to various OHCs (all: p<0.05; r: 0.43-0.96). Based on these relationships, we suggest that the OHC concentrations found in certain raptor chicks of Northern Scandinavia may impact blood plasma biochemistry in a way that indicates impacts on liver, kidney, bone, endocrinology and metabolism. In order to elaborate further on these relationships and mechanisms, we recommend that a larger study should take place in the near future.

Body feathers as a potential new biomonitoring tool in raptors: A study on organohalogenated contaminants in different feather types and preen oil of West Greenland white-tailed eagles (Haliaeetus albicilla)

We investigated the variation in concentrations and profiles of various classes of organohalogenated compounds (OHCs) in different feather types, muscle tissue and preen oil from 15 white-tailed eagle (Haliaeetus albicilla) carcasses from Greenland. The influence of moult patterns and potential external contamination onto the feather surface was examined, while the present study is also the first to investigate the use of body feathers for OHC monitoring. Concentrations of sum polychlorinated biphenyls (PCBs) in feathers from white tailed eagles ranged from 2.3 ng/g in a primary wing feather to 4200 ng/g in body feathers. Using 300 mg of body feathers, almost 50 different OHCs could be quantified and median concentrations in body feathers were 10 fold higher than concentrations in tail feathers (rectrices) or primary wing feathers. Body feathers could be very useful for biomonitoring taking into account their easy sampling, short preparation time and high levels of OHCs. In addition, the effects of confounding variables such as feather size, moult and age are also minimised using body feathers. Correlations with concentrations in muscle tissue and preen oil were high and significant for all feather types (r ranging from 0.81 to 0.87 for sum PCBs). Significant differences in concentrations and profiles of OHCs were found between different primary feathers, indicating that the accumulation of OHCs in feathers varies over the moulting period (maximum three years). Washing of feathers with an organic solvent (acetone) resulted in a significant decrease in the measured concentrations of OHCs in feathers. However, our results indicated that preen oil is probably not the only contributor to the external contamination that can be removed by washing with acetone. Possibly dust and other particles may be of importance and may be sticking to the preened feathers. Rectrices washed only with water showed high and significant correlations with concentrations in muscle and preen oil as well. Washing with acetone therefore does not seem to be of great influence when relating to internal tissue concentrations. We recommend washing feathers only with distilled water in order to remove dirt and dust particles before analysis.

A comparison of non-destructive sampling strategies to assess the exposure of white-tailed eagle nestlings (**Haliaeetus albicilla**) to persistent organic pollutants

To circumvent difficulties associated with monitoring adult predatory birds, we investigated the feasibility of different non-destructive strategies for nestling white-tailed eagles (Haliaeetus albicilla). We were able to quantify polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and organochlorinated pesticides (OCPs) in body feathers (16.92, 3.37 and 7.81ngg(-1) dw, respectively), blood plasma (8.37, 0.32 and 5.22ngmL(-1) ww, respectively), and preen oil (1157.95, 30.92 and 440.74ngg(-1) ww, respectively) of all nestlings (N=14). Strong significant correlations between blood plasma and preen oil concentrations (0.565≤r≤0.801; P<0.05) indicate that preen oil levels closely reflect the internal state of contamination. We found fewer significant correlations between body feather and blood plasma concentrations, which were almost exclusively between PCB concentrations (0.554≤r≤0.737; P<0.05). These results differ from a previous study on younger nestlings, and may indicate that the nestlings studied here, ready to fledge the nest, were possibly undergoing certain physiological changes that may have confounded the use of body feathers as biomonitor matrix. Finally, we provide an integrated discussion on the use of body feathers and preen oil as non-destructive biomonitor strategies for nestling predatory birds.

Persistent organic pollutants and methoxylated polybrominated diphenyl ethers in different tissues of white-tailed eagles (**Haliaeetus albicilla**) from West Greenland

We investigated polychlorinated biphenyls (PCBs), organochlorine pesticides (e.g. dichlorodiphenyltrichloroethane (DDT)), polybrominated diphenyl ethers (PBDEs) and methoxylated PBDEs (MeO-PBDEs), in six matrices (muscle, liver, kidney, adipose, blood, preen oil) of 17 white-tailed eagles from West Greenland sampled between 1997 and 2009. High inter-individual variation in contamination was found (PCBs: 0.49-1500 μg/g lipid weight (lw), DDTs: 0.23-910 μg/g lw, PBDEs: 0.01-24 μg/g lw, MeO-PBDEs: 0.001-0.59 μg/g lw), mostly due to age-related differences and not to temporal trends. One adult female (age > 5 years) displayed PCB levels up to 1500 μg/g lw in liver, which is the highest concentration ever reported in Arctic wildlife. Muscle generally contained the highest median levels, while adipose tissue displayed the lowest median levels on a lipid basis. No significant differences were found among tissues for MeO-PBDEs. Remarkably, we found distinct correlations (0.62 ≤ r ≤ 0.98; <0.0001 ≤ p ≤ 0.17) between levels of MeO-PBDEs and PBDEs, suggesting similar bioaccumulation pathways of PBDEs and MeO-PBDEs in white-tailed eagles.