Geir Wing Gabrielsen

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.

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 (Brünnichs 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.

Biomagnification of polybrominated diphenyl ether and hexabromocyclododecane flame retardants in the polar bear food chain in Svalbard, Norway.

Concentrations of brominated flame retardants (BFRs), including polybrominated diphenylethers (PBDEs) and hexabromocyclododecane (HBCD), were investigated in an arctic marine food chain consisting of four invertebrate species: polar cod (Boreogadus saida), ringed seals (Pusa hispida), and polar bears (Ursus maritimus). The most abundant BFR, brominated diphenyl ether (BDE)-47, was found in detectable concentrations even in zooplankton, the lowest trophic level examined in this study. Most of the investigated BFRs biomagnified as function of tropic level in the food chain. A noticeable exception occurred at the highest trophic level, the polar bear, in which only BDE-153 was found to increase from its main prey, the ringed seal, indicating that polar bears appear to be able to metabolize and biodegrade most BFRs. In contrast, lower-brominated PBDEs, particularly BDE-47, showed clear signs of bioaccumulation in zooplankton, polar cod, and ringed seals. We suggest that this discrepancy in the fate of BFRs among the different species may be related to greater induction of oxidative detoxification activities in the polar bear. Absorption and debromination rates may be more important for bioaccumulation rates of BFRs in zooplankton, polar cod, and ringed seals. Lipid weight-based concentrations (LWCs) and whole body-based concentrations (WBCs) of BFRs were used to assess biomagnification factors (BMFs). Whole-body concentrations gave the most realistic BMFs, as BMFs derived from LWCs seem to be confounded by the large variability in lipid content of tissues from the investigated species. This study demonstrates that PBDEs and HBCD have reached measurable concentrations even in the lower trophic levels (invertebrates and fish) in the Arctic and biomagnifies in the polar bear food chain.

Stroke and glide of wing-propelled divers: deep diving seabirds adjust surge frequency to buoyancy change with depth

In order to increase locomotor efficiency, breath–holding divers are expected to adjust their forward thrusts in relation to changes of buoyancy with depth. Wing propulsion during deep diving by Brünnichs guillemots (Uria lomvia) was measured in the wild by high–speed (32 Hz) sampling of surge (tail–to–head) and heave (ventral–to–dorsal) accelerations with bird–borne data loggers. At the start of descent, the birds produced frequent surges (3.2 Hz) during both the upstroke and the downstroke against buoyancy to attain a mean speed of 1.2–1.8 m s–1 that was close to the expected optimal swim speed. As they descended deeper, the birds decreased the frequency of surges to 2.4 Hz, relaying only on the downstroke. During their ascent, they stopped stroking at 18 m depth, after which the swim speed increased to 2.3 m s–1, possibly because of increasing buoyancy as air volumes expanded. This smooth change of surge frequency was achieved while maintaining a constant stroke duration (0.4–0.5 s), presumably allowing efficient muscle contraction.

Modulation of prolactin but not corticosterone responses to stress in relation to parental effort in a long-lived bird

We tested the hypothesis that parental effort modulates the magnitude of corticosterone and prolactin responses to stress in a long-lived bird, the Black-legged kittiwake (Rissa tridactyla). To do so, we compared corticosterone and prolactin responses to capture/restraint stress between chick-rearing birds and failed breeders (no parental effort). We predicted that (1) the increase in plasma corticosterone levels in response to stress should be lower in chick-rearing birds, (2) the decrease in plasma prolactin levels in response to stress should be lower in chick-rearing birds, and (3) as both sexes care for the chick, there should be no sex difference in the hormonal response to stress. Baseline plasma corticosterone and prolactin levels were higher in chick-rearing birds and were not influenced by body condition. Failed breeders were in better condition than chick-rearing individuals. Corticosterone response to stress was unaffected by parental effort as both chick-rearing and failed birds exhibited a robust corticosterone increase. Prolactin response to stress was however clearly influenced by parental effort: chick-rearing birds showed a modest 9% prolactin decrease whereas in failed birds prolactin concentrations fell by 41%. Body condition did not influence hormonal responses to stress. When facing stressful condition, breeding kittiwakes attenuate their prolactin response to stress while enhancing their secretion of corticosterone. Increasing corticosterone secretion triggers foraging efforts and diminishes nest attendance whereas an attenuation of prolactin response to stress maintains parental behavior. We suggest that this hormonal mechanism facilitates a flexible time-budget that has been interpreted as a buffer against environmental variability.

Repeatability of basal metabolism in breeding female kittiwakes Rissa tridactyla

We studied kittiwakes (Rissa tridactyla) breeding near Ny–Ålesund (79° N, 12° E) on Svalbard. In 1997, the basal metabolic rates (BMRs) of 17 breeding females were measured during the incubation and chick–rearing periods. The mean body mass of the kittiwakes decreased significantly (by 10%) between the incubation and chick–rearing periods. At the same time, both the whole–body and mass–specific BMRs decreased significantly. There was a positive and significant relationship between the BMR residuals from the incubation period and those from the chick–rearing period. Thus, the BMR of incubating female kittiwakes is a significant predictor of their BMR during the chick–rearing period. New BMR data were collected in 1998 from ten of these females, measured around the chick–hatching date. Repeatability values were calculated using either (i) the data for eight individuals for which three BMR measurements existed, or (ii) all the data from both years, yielding significant repeatabilities of 0.52 and 0.35, respectively. These values indicate that between 48 and 65% of the observed variation in BMR is due to intraindividual variability, while between–individual variability accounts for 35–52% of the variation in the BMR. This is the first report of a significant repeatability of the BMR of an endothermic organism across an elapsed time of more than one day.

Cadmium, zinc, copper, arsenic, selenium and mercury in seabirds from the Barents Sea: levels, inter-specific and geographical differences

Trace elements Cd, Zn, Cu, As, Se and Hg were analysed in muscle and liver of Brünnichs guillemot, Common guillemot, Puffin, Black guillemot, Little auk, Razorbill, Common eider, King eider, Glaucous gull, Herring gull, Black-legged kittiwake, Northern fulmar and Arctic tern collected in 1991-1992 at the main breeding colonies in the Barents Sea. The highest levels of the most toxic elements Cd and Hg were found in birds nesting north of Spitsbergen. Extremely high levels of As were detected in tissues of all seabird species collected at colonies in Chernaya Guba (Novaya Zemlya), where nuclear tests were carried out in the 1960s. In general, levels of all of the trace elements in the Barents Sea seabirds were similar or lower in comparison with those reported for the same seabird species from the other Arctic areas. Data on metallothionein concentrations in different seabird species need to be collected in order to understand the mechanism of bioaccumulation and possible toxic effects of trace elements in Arctic seabirds.

Biomagnification of mercury in selected species from an Arctic marine food web in Svalbard

Concentrations and biomagnification of total mercury (TotHg) and methyl mercury (MeHg) were studied in selected species from the pelagic food web in Kongsfjorden, Svalbard. Twelve species of zooplankton, fish and seabirds, were sampled representing a gradient of trophic positions in the Svalbard marine food web. TotHg and MeHg were analysed in liver, muscle and/or whole specimens. The present study is the first to provide MeHg levels in seabirds from the Svalbard area. The relative MeHg levels decreased with increasing levels of TotHg in seabird tissues. Stable isotopes of nitrogen (delta(15)N) were used to determine the trophic levels and the rate of biomagnification of mercury in the food web. A linear relationship between mercury levels and trophic position was found for all seabird species combined and their trophic level, but there was no relationship within species. Biomagnification factors were all >1 for both TotHg and MeHg, indicating biomagnification from prey to predator. TotHg levels in the different seabirds were similar to levels detected in the Kongsfjorden area in the 1990s.

Validation of the use of blood samples to assess tissue concentrations of organochlorines in glaucous gulls, Larus hyperboreus

Abstract Fifteen adult glaucous gulls, Larus hyperboreus, were captured near Ny-Alesund, Svalbard. The birds were kept in captivity for 24–41 days and fed a diet of polar cod, Boreogadus saida. A range of organochlorines (OCs) were quantified in blood, brain, liver, and subcutaneous fat tissue. For more than 80% of the quantified OCs, r2 values >0.75 were found for the blood-liver concentration correlations. Repeated sampling revealed intra-individual temporal variability in blood OC concentrations. Much of the temporal variability in OC blood concentrations was associated with changes in nutritional condition.

Corticosterone and time-activity budget: An experiment with Black-legged kittiwakes

In vertebrates, the well established increase in plasma corticosterone in response to food shortage is thought to mediate adjustments of foraging behavior and energy allocation to environmental conditions. However, investigating the functional role of corticosterone is often constrained by the difficulty to track time-activity budget of free-ranging animals. To examine how an experimental increase in corticosterone affects the activity budget of male Black-legged kittiwakes (Rissa tridactyla), we used miniaturized activity loggers to record flying/foraging, presence on the sea surface and nest attendance. To investigate how corticosterone affects allocation processes between self-foraging and foraging devoted to the brood, we monitored body mass change of males from capture (day 0) to recapture (day 3). Among control birds, males in poor condition at day 0 spent significantly more time flying/foraging and less time attending the nest site than did males in good condition. Corticosterone treatment affected time spent flying/foraging in interaction with body condition at day 0: corticosterone-implanted males in good condition spent more time flying/foraging than control ones; this was not observed in poor condition males. In control birds, change in body mass was negatively correlated with body condition at day 0. This was reinforced by corticosterone treatment and, on average, corticosterone-implanted males gained much more mass than controls. These results suggest that in Black-legged kittiwakes, body condition and corticosterone levels can interact to mediate foraging decisions and possibly energy allocation: when facing stressful environmental conditions, birds in good body condition may afford to increase the time spent foraging probably to maintain brood provisioning, whereas poor body condition birds seemed rather to redirect available energy from reproduction to self-maintenance.