Jan Ove Bustnes

Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish

Persistent organic pollutants (POPs) encompass an array of anthropogenic organic and elemental substances and their degradation and metabolic byproducts that have been found in the tissues of exposed animals, especially POPs categorized as organohalogen contaminants (OHCs). OHCs have been of concern in the circumpolar arctic for decades. For example, as a consequence of bioaccumulation and in some cases biomagnification of legacy (e.g., chlorinated PCBs, DDTs and CHLs) and emerging (e.g., brominated flame retardants (BFRs) and in particular polybrominated diphenyl ethers (PBDEs) and perfluorinated compounds (PFCs) including perfluorooctane sulfonate (PFOS) and perfluorooctanic acid (PFOA) found in Arctic biota and humans. Of high concern are the potential biological effects of these contaminants in exposed Arctic wildlife and fish. As concluded in the last review in 2004 for the Arctic Monitoring and Assessment Program (AMAP) on the effects of POPs in Arctic wildlife, prior to 1997, biological effects data were minimal and insufficient at any level of biological organization. The present review summarizes recent studies on biological effects in relation to OHC exposure, and attempts to assess known tissue/body compartment concentration data in the context of possible threshold levels of effects to evaluate the risks. This review concentrates mainly on post-2002, new OHC effects data in Arctic wildlife and fish, and is largely based on recently available effects data for populations of several top trophic level species, including seabirds (e.g., glaucous gull (Larus hyperboreus)), polar bears (Ursus maritimus), polar (Arctic) fox (Vulpes lagopus), and Arctic charr (Salvelinus alpinus), as well as semi-captive studies on sled dogs (Canis familiaris). Regardless, there remains a dearth of data on true contaminant exposure, cause-effect relationships with respect to these contaminant exposures in Arctic wildlife and fish. Indications of exposure effects are largely based on correlations between biomarker endpoints (e.g., biochemical processes related to the immune and endocrine system, pathological changes in tissues and reproduction and development) and tissue residue levels of OHCs (e.g., PCBs, DDTs, CHLs, PBDEs and in a few cases perfluorinated carboxylic acids (PFCAs) and perfluorinated sulfonates (PFSAs)). Some exceptions include semi-field studies on comparative contaminant effects of control and exposed cohorts of captive Greenland sled dogs, and performance studies mimicking environmentally relevant PCB concentrations in Arctic charr. Recent tissue concentrations in several arctic marine mammal species and populations exceed a general threshold level of concern of 1 part-per-million (ppm), but a clear evidence of a POP/OHC-related stress in these populations remains to be confirmed. There remains minimal evidence that OHCs are having widespread effects on the health of Arctic organisms, with the possible exception of East Greenland and Svalbard polar bears and Svalbard glaucous gulls. However, the true (if any real) effects of POPs in Arctic wildlife have to be put into the context of other environmental, ecological and physiological stressors (both anthropogenic and natural) that render an overall complex picture. For instance, seasonal changes in food intake and corresponding cycles of fattening and emaciation seen in Arctic animals can modify contaminant tissue distribution and toxicokinetics (contaminant deposition, metabolism and depuration). Also, other factors, including impact of climate change (seasonal ice and temperature changes, and connection to food web changes, nutrition, etc. in exposed biota), disease, species invasion and the connection to disease resistance will impact toxicant exposure. Overall, further research and better understanding of POP/OHC impact on animal performance in Arctic biota are recommended. Regardless, it could be argued that Arctic wildlife and fish at the highest potential risk of POP/OHC exposure and mediated effects are East Greenland, Svalbard and (West and South) Hudson Bay polar bears, Alaskan and Northern Norway killer whales, several species of gulls and other seabirds from the Svalbard area, Northern Norway, East Greenland, the Kara Sea and/or the Canadian central high Arctic, East Greenland ringed seal and a few populations of Arctic charr and Greenland shark.

ECOLOGICAL EFFECTS OF ORGANOCHLORINE POLLUTANTS IN THE ARCTIC: A STUDY OF THE GLAUCOUS GULL

Since the early 1970s, high levels of long-transported organochlorine pollutants (OCs) such as PCBs and DDE have been found in seabirds in the European Arctic, especially in the Glaucous Gull, Larus hyperboreus. However, the potential ecological effects of these contaminants have not been studied. We measured the concentrations of 15 different OCs (HCB, three HCHs, oxychlordane, DDE, and nine PCB congeners) in the blood of 111 Glaucous Gulls and related the concentrations to fitness components of the same individuals. Blood samples were taken in 1997, and individuals were followed until 2000. We first conducted a principal component analysis (PCA) on all OCs and related reproductive traits and survival to the first and second PCA axes, which represented persistent compounds and more volatile compounds, respectively. We then related reproductive traits and survival to all OCs separately, except for persistent PCB congeners (for which we used their sum), to test if some compounds were more consistently related to negative fitness effects than others. Females with high circulating levels of persistent OCs were more likely to lay nonviable eggs than were females with low levels, whereas levels of more volatile OCs were not related to egg viability. Moreover, there was a negative relationship between PC1, in addition to female blood concentration of both persistent and some volatile OCs, and the hatching condition of the chick from the first egg laid in clutches. The hatching condition of the second chick in clutches was significantly negatively related to PC1, and specifically to female blood concentrations of HCB, β-HCH, and PCB-28. Apart from a negative association between OC concentrations and laying date in both sexes, no other reproductive parameters (clutch size, egg size, incubation time, nest predation, and early chick survival) showed associations with any of the OCs measured. Hence, reproductive effects were most likely related to maternal transfer of persistent OCs to eggs. Adult survival was negatively related to blood concentration of DDE, persistent PCBs and HCB, and especially to oxychlordane. Survival probability was reduced by 29% in females and 16% in males as oxychlordane concentrations in the blood increased 10-fold (from 5 to 50 ng/g wet mass). In long-lived birds, adult survival probability is the parameter to which the population growth rate is most sensitive, suggesting that persistent OCs have the potential for causing considerable effects on the population dynamics of Arctic-breeding Glaucous Gulls. Corresponding Editor: D. J. Levey.

To breed or not to breed: endocrine response to mercury contamination by an Arctic seabird

Mercury, a ubiquitous toxic element, is known to alter expression of sex steroids and to impair reproduction across vertebrates but the mechanisms underlying these effects are not clearly identified. We examined whether contamination by mercury predicts the probability to skip reproduction in black-legged kittiwakes (Rissa tridactyla) from Svalbard. We also manipulated the endocrine system to investigate the mechanism underlying this relationship. During the pre-laying period, we injected exogenous GnRH (gonadotropin-releasing hormone) to test the ability of the pituitary to release luteinizing hormone (LH, a key hormone for the release of sex steroids and hence breeding) in relation to mercury burden. Birds that skipped reproduction had significantly higher mercury concentration in blood than breeders. Endocrine profiles of these birds also varied based on breeding status (breeders versus non-breeders), mercury contamination and sex. Specifically, in skippers (birds that did not breed), baseline LH decreased with increasing mercury concentration in males, whereas it increased in females. GnRH-induced LH levels increased with increasing mercury concentration in both sexes. These results suggest that mercury contamination may disrupt GnRH input to the pituitary. Thus, high mercury concentration could affect the ability of long-lived birds to modulate their reproductive effort (skipping or breeding) according to ongoing environmental changes in the Arctic, thereby impacting population dynamics.

Differential investment and costs during avian incubation determined by individual quality: an experimental study of the common eider (Somateria mollissima)

Individuals of different quality may have different investment strategies, shaping responses to experimental manipulations, thereby rendering the detection of such patterns difficult. However, previous clutch–size manipulation studies have infrequently incorporated individual differences in quality. To examine costs of incubation and reproductive investment in relation to changes in clutch size, we enlarged and reduced natural clutch sizes of four and five eggs by one egg early in the incubation period in female common eiders (Somateria mollissima), a sea duck with an anorectic incubation period. Females that had produced four eggs (lower quality) responded to clutch reductions by deserting the nest more frequently but did not increase incubation effort in response to clutch enlargement, at the cost of reduced hatch success of eggs. Among birds with an original clutch size of five (higher quality), reducing and enlarging clutch size reduced and increased relative body mass loss respectively without affecting hatch success. In common eiders many females abandon their own ducklings to the care of other females. Enlarging five–egg clutches led to increased brood care rate despite the higher effort spent incubating these clutches, indicating that the higher fitness value of a large brood is increasing adult brood investment. This study shows that the ability to respond to clutch–size manipulations depends on original clutch size, reflecting differences in female quality. Females of low quality were reluctant to increase investment at the cost of lower hatch success, whereas females of higher quality apparently have a larger capacity both to increase incubation effort and brood care investment.

Costs of reproduction in common eiders ( Somateria mollissima ): An assessment of relationships between reproductive effort and future survival and reproduction based on observational and experimental studies

The two traditional approaches to the study of costs of reproduction, correlational and experimental, have been used in parallel in a breeding colony of common eiders ( Somateria mollissima ) and were compared in this paper. The analysis of the observational data was based on a two-strata capture-recapture model, the strata being defined on the basis of the clutch size laid by individual females in a given year. The best model according to AIC C indicated substantial variation in survival, recapture and transition rates, but overall a pattern emerged: females laying large clutches have a somewhat higher survival and much higher capture rate than females laying small clutches, and transition from large to small clutch size occurs much more frequently than the reverse transition. The analysis of the experimental data (adding/removing one egg) showed that no clear effect was found on either survival or transition rates. We conclude by suggesting (1) that condition should be included in multi-strata models in addition to reproductive effort; (2) that a specific study design for estimating the proportion of non-breeding females should be implemented, and (3) that non-breeding (a non-observable state in this study) may be influenced by previous reproduction events.

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.

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.

BEHAVIORAL RESPONSES TO DECREASING DAY LENGTH IN WINTERING SEA DUCKS

Abstract Sea ducks generally are diurnal feeders, but large numbers winter above the Arctic Circle where day lengths decrease dramatically in winter. To determine how sea ducks cope with short day lengths, we studied different aspects of the behavior of three sympatric wintering species (Common Eider [Somateria mollissima], King Eider [S. spectabilis], and Oldsquaw [Clangula hyemalis]) at 70°N where day length is reduced to less than 4.5 h of twilight in midwinter. Numbers of both eider species remained fairly constant throughout winter, whereas Oldsquaws moved out of the area in midwinter. As day length decreased, eiders extended their feeding period into lower light intensities. Common Eiders and Oldsquaws spent a higher proportion of the day diving (underwater) when days were short, whereas King Eiders did not. As the days lengthened, King Eiders and Oldsquaws increased their total time diving at similar rates, which were faster than those of Common Eiders. Feeding at lower light intensities and increased proportions of time spent diving did not offset reduced feeding time in midwinter, and estimated time spent underwater during daylight on the shortest days was only 35% of that on the longest days in King Eiders, 51% in Common Eiders, and 39% in Oldsquaws. The ability to survive when days are short might be explained by use of stored nutrient reserves, night feeding, or high prey availability.

Corticosterone, prolactin and egg neglect behavior in relation to mercury and legacy POPs in a long-lived Antarctic bird

Seabirds often have high loads of contaminants. These contaminants have endocrine disrupting properties but their relationships with some endocrine mechanisms are still poorly investigated in free-living organisms. This is the case for the stress response which shifts energy investment away from reproduction and redirects it towards survival. In birds, this stress response is achieved through a release of corticosterone and is also accompanied by a decrease in circulating prolactin, an anterior pituitary hormone widely involved in regulating parental cares. We measured blood concentrations of some legacy persistent organic pollutants (POPs) and mercury (Hg) and examined their relationships with the corticosterone and prolactin responses of known-age (9-46 years old) incubating snow petrels (Pagodroma nivea) to a standardized capture/handling stress protocol. In this Antarctic seabird, we also investigated whether high contaminant burden correlates with a higher occurrence of egg neglect, a frequently observed behavior in snow petrels. POPs and Hg were unrelated to age. Stress-induced corticosterone concentrations were positively related to POPs in both sexes, and stress-induced prolactin concentrations were negatively related to Hg in males. Egg-neglect behavior was not related to POPs burden, but males with higher Hg concentrations were more likely to neglect their egg. This suggests that in birds, relationships between age and contaminants are complex and that even low to moderate concentrations of POPs and Hg are significantly related to hormonal secretion. In this Antarctic species, exposure to legacy POPs and Hg could make individuals more susceptible to environmental stressors such as ongoing disturbances in Polar Regions.

Temporal trends and pattern of polyfluoroalkyl compounds in Tawny Owl (Strix aluco) eggs from Norway, 1986-2009.

Temporal trends of polyfluoroalkyl compounds (PFCs) were examined in tawny owl (Strix aluco) eggs collected in Central Norway over a period of 24 years (1986-2009). Concentrations of 12 PFCs, including C(6)-C(8), C(10) perfluoroalkyl sulfonates (PFSAs), perfluorooctane sulfonamide (PFOSA), and C(8)-C(14) perfluoroalkyl carboxylates (PFCAs), were measured, whereas saturated and unsaturated fluorotelomer carboxylates and shorter chain PFSAs and PFCAs were not detected. Perfluorooctane sulfonate (PFOS) was the predominant compound (geometric mean 10.1 ng/g wet weight (ww)), followed by perfluorotridecanoate (PFTriDA) (0.36 ng/g ww) and perfluoroundecanoate (PFUnDA) (0.19 ng/g ww). Significant decreasing concentrations were found for PFOS with an annual decrease of 1.6% (1986-2009), while, conversely, the C(10)-C(13) PFCA concentrations increase significantly with an annual increase of 4.2-12% (1986-2009). Consequently, the contribution of PFOS to the ∑PFCs decreased, whereas the contribution of the ∑PFCAs increased over the time. Toxicological implications for tawny owls are limited, but the maximal PFOS concentration found in this stu0dy is about 20 times lower than the predicted avian no effect concentration (PNEC) which suggest adverse effects caused by PFOS are unlikely. However, tawny owls are exposed to a mixture of various PFCs, and PFCA concentrations still increase.