Do foraging ecology and contaminants interactively predict parenting hormone levels in common eider?

Global climate change is causing abiotic shifts such as higher air and ocean temperatures, and disappearing sea ice in Arctic ecosystems. These changes influence Arctic-breeding seabird foraging ecology by altering prey availability and selection, affecting individual body condition, reproductive success, and exposure to contaminants such as mercury (Hg). The cumulative effects of alterations to foraging ecology and Hg exposure may interactively alter the secretion of key reproductive hormones such as prolactin (PRL), important for parental attachment to eggs and offspring and overall reproductive success. However, more research is needed to investigate the relationships between these potential links. Using data collected from 106 incubating female common eiders (Somateria mollissima) at six Arctic and sub-Arctic colonies, we examined whether the relationship between individual foraging ecology (assessed using δ13C, δ15N) and total Hg (THg) exposure predicted PRL levels. We found a significant, complex interaction between δ13C, δ15N and THg on PRL, suggesting that individuals cumulatively foraging at lower trophic levels, in phytoplankton-dominant environments, and with the highest THg levels had the most constant significant relationship PRL levels. Cumulatively, these three interactive variables resulted in lowered PRL. Overall, results demonstrate the potential downstream and cumulative implications of environmentally induced changes in foraging ecology, in combination with THg exposure, on hormones known to influence reproductive success in seabirds. These findings are notable in the context of continuing environmental and food web changes in Arctic systems, which may make seabird populations more susceptible to ongoing stressors.

Environmental and life-history factors influence inter-colony multidimensional niche metrics of a breeding Arctic marine bird.

Human industrialization has resulted in rapid climate change, leading to wide-scale environmental shifts. These shifts can modify food web dynamics by altering the abundance and distribution of primary producers (ice algae and phytoplankton), as well as animals at higher trophic levels. Methylmercury (MeHg) is a neuro-endocrine disrupting compound which biomagnifies in animals as a function of prey choice, and as such bioavailability is affected by altered food web dynamics and adds an important risk-based dimension in studies of foraging ecology. Multidimensional niche dynamics (MDND; δ13C, δ15N, THg; total mercury) were determined among breeding common eider (Somateria mollissima) ducks sampled from 10 breeding colonies distributed across the circumpolar Arctic and subarctic. Results showed high variation in MDND among colonies as indicated by niche size and ranges in δ13C, δ15N and THg values in relation to spatial differences in primary production inferred from sea-ice presence and colony migratory status. Colonies with higher sea-ice cover during the pre-incubation period had higher median colony THg, δ15N, and δ13C. Individuals at migratory colonies had relatively higher THg and δ15N, and lower δ13C, suggesting a higher trophic position and a greater reliance on phytoplankton-based prey. It was concluded that variation in MDND exists among eider colonies which influenced individual blood THg concentrations. Further exploration of spatial ecotoxicology and MDND at each individual site is important to examine the relationships between anthropogenic activities, foraging behaviour, and the related risks of contaminant exposure at even low, sub-lethal concentrations that may contribute to deleterious effects on population stability over time. Overall, multidimensional niche analysis that incorporates multiple isotopic and contaminant metrics could help identify those populations at risk to rapidly altered food web dynamics.

Multiple Stressors in a Top Predator Seabird: Potential Ecological Consequences of Environmental Contaminants, Population Health and Breeding Conditions.

Environmental contaminants may have impacts on reproduction and survival in wildlife populations suffering from multiple stressors. This study examined whether adverse effects of persistent organic pollutants (POPs) increased with poor population health and breeding conditions in three colonies (60-74°N) of great skua (Stercorarius skua) in the north-eastern Atlantic (Shetland, Iceland and Bjørnøya [Bear Island]). POPs (organochlorines [OCs] and polybrominated diphenyl ethers [BDEs]) were measured in plasma of incubating birds (n = 222), concentrations differing nearly tenfold among colonies: Bjørnøya (2009) > Bjørnøya (2010) > Iceland (2009) > Shetland (2009). Reproductive success (hatching success and chick survival) showed that breeding conditions were favourable in Shetland and at Bjørnøya (2010), but were very poor in Iceland and at Bjørnøya (2009). Biomarkers indicated that health was poor in the Shetland population compared to the other populations. Females whose chicks hatched late had high POP concentrations in all colonies except at Bjørnøya (2010), and females losing their eggs at Bjørnøya (2009) tended to have higher concentrations than those hatching. Moreover, there was a negative relationship between female POP concentrations and chick body condition at hatching in Iceland and at Bjørnøya (2010). Supplementary feeding experiments were conducted, and in Iceland where feeding conditions were poor, significant negative relationships were found between female POP concentrations and daily growth-rate in first-hatched chicks of control nests, but not in food supplemented nests. This suggests that negative impacts of POPs were mitigated by improved feeding conditions. For second-chicks, there was a strong negative relationship between the female POP concentrations and growth-rate, but no effects of supplementary feeding. Lowered adult return-rate between breeding seasons with increasing POP loads were found both at Bjørnøya (2009) and in Shetland, especially related to BDEs. This indicates stronger fitness consequences of POPs following seasons with very poor breeding conditions and/or high reproductive effort. This study suggests that the impacts of POPs may differ depending on population health and breeding conditions, and that even low concentrations of POPs could have ecological consequences during adverse circumstances. This is important with regard to risk assessment of biomagnifying contaminants in marine ecosystems.

Avian influenza virus ecology in Iceland shorebirds: intercontinental reassortment and movement.

Shorebirds are a primary reservoir of avian influenza viruses (AIV). We conducted surveillance studies in Iceland shorebird populations for 3 years, documenting high serological evidence of AIV exposure in shorebirds, primarily in Ruddy Turnstones (Arenaria interpres; seroprevalence=75%). However, little evidence of virus infection was found in these shorebird populations and only two turnstone AIVs (H2N7; H5N1) were able to be phylogenetically examined. These analyses showed that viruses from Iceland shorebirds were primarily derived from Eurasian lineage viruses, yet the H2 hemagglutinin gene segment was from a North American lineage previously detected in a gull from Iceland the previous year. The H5N1 virus was determined to be low pathogenic, however the PB2 gene was closely related to the PB2 from highly pathogenic H5N1 isolates from China. Multiple lines of evidence suggest that the turnstones were infected with at least one of these AIV while in Iceland and confirm Iceland as an important location where AIV from different continents interact and reassort, creating new virus genomes. Mounting data warrant continued surveillance for AIV in wild birds in the North Atlantic, including Canada, Greenland, and the northeast USA to determine the risks of new AI viruses and their intercontinental movement in this region.

Feather corticosterone levels on wintering grounds have no carry-over effects on breeding among three populations of great skuas (Stercorarius skua).

Environmental conditions encountered by migratory seabirds in their wintering areas can shape their fitness. However, the underlying physiological mechanisms remain largely unknown as birds are relatively inaccessible during winter. To assess physiological condition during this period, we measured corticosterone concentrations in winter-grown primary feathers of female great skuas (Stercorarius skua) from three breeding colonies (Bjørnøya, Iceland, Shetland) with wintering areas identified from characteristic stable isotope signatures. We subsequently compared winter feather corticosterone levels between three wintering areas (Africa, Europe and America). Among females breeding in 2009, we found significant differences in feather corticosterone levels between wintering areas. Surprisingly, levels were significantly higher in Africa despite seemingly better local ecological factors (based on lower foraging effort). Moreover, contrary to our predictions, females sharing the same wintering grounds showed significant differences in feather corticosterone levels depending on their colony of origin suggesting that some skuas could be using suboptimal wintering areas. Among females wintering in Africa, Shetland females showed feather corticosterone levels on average 22% lower than Bjørnøya and Iceland females. Finally, the lack of significant relationships between winter feather corticosterone levels and any of the breeding phenology traits does not support the hypothesis of potential carry-over effects of winter feather corticosterone. Yet, the fitness consequences of elevated feather corticosterone levels remain to be determined.

Organohalogen contaminants and Blood plasma clinical-chemical parameters in three colonies of North Atlantic Great skua (Stercorarius skua).

The present study compares blood plasma clinical-chemical parameters (BCCPs) in birds from three geographically distinct North Atlantic Great skua (Stercorarius skua) colonies. Birds from these sites bioaccumulate different POP (persistent organic pollutant) concentrations and that enabled us to compare Great skua BCCPs in different exposure scenarios. Persistent organic pollutants (organochlorines: PCB, DDT, chlordanes, HCB, HCH, mirex and brominated flame retardants: PBDEs) and nineteen BCCPs were analysed in 114 adult Great skuas sampled during summer 2009 in North Atlantic colonies at Bjørnøya (n=42), Iceland (n=57) and Shetland (n=15). Specimens from Bjørnøya had the highest blood plasma concentrations of all contaminant groups followed by Iceland and Shetland birds, respectively (ANOVA: p<0.05). Most of the 19 BCCP parameters followed the pattern of colony differences found for contaminants, with Bjørnøya having the highest concentrations. However seven BCCPs, the three liver enzymes ALKP, ALAT and GGT as well as bile acids, cholesterol, sodium and potassium, did not differ between colonies (ANOVA: p>0.05). Therefore correlation analyses of these seven BCCPs vs. POPs were done on the combined colony data while the analyses of the remaining 12 BCCPs were carried out for each colony separately. The analyses of combined colony data showed that the blood plasma concentration of liver enzymes ALAT and GGT increased with increasing concentrations of ΣPBDE and ΣHCH, HCB and ΣCHL, respectively (all Pearson's p<0.05). In Great skuas from Shetland, the important osmotic transport protein albumin increased with increasing concentrations of ΣPCB and ΣDDT, while total blood plasma protein increased with ΣPCB, ΣDDT, ΣHCH and HCB concentrations (all Pearson's p<0.05). In both Bjørnøya and Iceland skuas, blood plasma pancreatic enzyme amylase decreased with increasing ΣHCH concentrations while the erythrocyte waste product total bilirubin in blood plasma increased with increasing ΣHCH and ΣPBDE concentrations in Iceland Great skuas (all Pearson's p<0.05). In Bjørnøya birds, blood plasma urea from protein metabolism (reflects kidney function) increased with increasing ΣPBDE concentrations (Pearson's p<0.05). Furthermore, a redundancy analysis showed that 10.6% of the variations in BCCPs could be explained by the variations in POP concentrations. Based on these results we suggest that liver and renal functions could be negatively affected by different POP compounds. It is, however, uncertain if the colony BCCP differences and their relationship to POP concentrations reflect health effects that could have an overall impact on the populations via reduced survival and reproduction parameters.

Individual variation in biomarkers of health: influence of persistent organic pollutants in Great skuas (Stercorarius skua) breeding at different geographical locations.

Persistent organic pollutants (POPs) have been shown to cause adverse effects on a number of biomarkers of health in birds. POPs may impair immune function and alter the stress response, defined as a suite of behavioral and physiological responses to environmental perturbations. Recent studies have also proposed that POPs can induce oxidative stress. Nevertheless, there is a lack of studies simultaneously assessing the potential damaging effects of POPs on the latter biomarkers. In this study, we examined the contribution of legacy (organochlorines; (OCs)) and emerging (flame retardants; PBDEs) POPs to individual variations in stress levels (feather corticosterone), humoral immunity (plasma immunoglobulin Y levels) and oxidative stress occurring in three breeding colonies of a top predator seabird, the Great skua (Stercorarius skua), distributed from temperate regions to the high Arctic: Shetland (60°N), Iceland (63°N) and Bjørnøya (74°N). Our results demonstrated that plasma concentrations of OCs in Great skuas from Bjørnøya are among the highest in North Atlantic seabirds, with up to 7900 µg/kg (ww) ∑OCs. Yet, a latitudinal gradient in POP levels was observed with all compounds being significantly higher in Bjørnøya than in Iceland and Shetland (on average 4-7 fold higher for OCs and 2.5-4.5 for PBDEs, respectively). Contrary to our predictions, skuas breeding at the least contaminated site (i.e., Shetland) experienced the poorest physiological condition; i.e., the highest levels of stress hormones (25% higher) and oxidative stress (50% higher) and the lowest immunoglobulin levels (15% lower) compared to the two other colonies. Finally, our results failed to point out consistent within-colony relationships between biomarkers of health and POPs. Overall, it is suggested that other ecological factors such as food availability could constrain physiological indicators more than anthropogenic contaminants.

Effects of environmental exposure and diet on levels of persistent organic pollutants (POPs) in eggs of a top predator in the North Atlantic in 1980 and 2008.

Concentrations of POPs in Great skua eggs from Shetland are among the highest in North Atlantic seabirds, with up to 11,600 µg/kg (ww) DDE and up to 17,900 µg/kg ww ∑PCB. Concentrations of legacy POPs were significantly lower in 2008 than 1980. Decreases were greatest for least persistent compounds. Median ∑PBDEs increased from 99 µg/kg ww in 1980 to 173 µg/kg ww in 2008. There were changes in Great skua breeding season diet, with more adult Herring and Mackerel and less Sandeel. These changes increase exposure to POPs, since Herring and Mackerel accumulate more POPs than Sandeels. In both years, eggs with higher δ15N had higher POP concentrations. In 1980, birds feeding more on demersal discard fish from trawl fisheries and less on Sandeels, had higher POP levels in eggs. In 2008, individuals feeding more on Herring and Mackerel, and less on discards, had higher POP levels in eggs.