Direct evidence of a prey depletion "halo" surrounding a pelagic predator colony.

Colonially breeding birds and mammals form some of the largest gatherings of apex predators in the natural world and have provided model systems for studying mechanisms of population regulation in animals. According to one influential hypothesis, intense competition for food among large numbers of spatially constrained foragers should result in a zone of prey depletion surrounding such colonies, ultimately limiting their size. However, while indirect and theoretical support for this phenomenon, known as "Ashmole's halo," has steadily accumulated, direct evidence remains exceptionally scarce. Using a combination of vessel-based surveys and Global Positioning System tracking, we show that pelagic seabirds breeding at the tropical island that first inspired Ashmole's hypothesis do indeed deplete their primary prey species (flying fish; Exocoetidae spp.) over a considerable area, with reduced prey density detectable >150 km from the colony. The observed prey gradient was mirrored by an opposing trend in seabird foraging effort, could not be explained by confounding environmental variability, and can be approximated using a mechanistic consumption-dispersion model, incorporating realistic rates of seabird predation and random prey dispersal. Our results provide a rare view of the resource footprint of a pelagic seabird colony and reveal how aggregations of these central-place foraging, marine top predators profoundly influence the oceans that surround them.

The effect of long-range transport, trophic position and diet specialization on legacy contaminant occurrence in great skuas, Stercorarius skua, breeding across the Northeast Atlantic.

High levels of halogenated organic contaminants (HOCs) have been found in the marine predatory seabird great skua (Stercorarius skua) from breeding colonies in the Northeastern Atlantic, with large unexplained inter-colony variation. The present study aimed at analyzing if the HOCs occurrence in breeding great skuas in remote colonies was explained by local baseline food web exposure determined by long-range transport, or by ecological factors such as diet specialization and relative trophic position in the breeding area. The occurrence of organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs) was analyzed in plasma of 204 adult great skuas collected over two years (2008 and 2009) and 5 colonies across the North-Atlantic from Shetland to Svalbard. The ΣHOCs levels in plasma ranged across two orders of magnitude, from 40 to 7600 ng/g (wet weight) and differed significantly across the great skua colonies. The variation in contaminant occurrence among colonies did not reflect long-range transport through a latitudinal or remoteness gradient, as the second northernmost colony (Bjørnøya), had the highest contaminant concentrations. No latitudinal or remoteness gradient was evident in the contaminant pattern among the colonies. The contaminant levels increased significantly with increasing δ15N values, and regurgitated pellets of undigested prey suggested that great skuas with higher δ15N values had a higher proportion of bird prey in their diet, mostly seabirds. In contrast, great skuas from colonies with lower δ15N and lower contaminant level fed mostly on fish. The enrichment of δ13C increased with decreasing δ15N and lower contaminant levels. Therefore, individual behavior of great skuas, such as migration strategies and diet specialization, rather than long-range transport and thus baseline food web exposure, explain among and within colony variance in contaminant occurrence.

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.

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.

Dietary versus maternal sources of organochlorines in top predator seabird chicks: an experimental approach.

We examined the relative importance of dietary sources and maternal transfer on organochlorine concentrations (∑OCs) in Great skua chicks (Stercorarius skua) in Shetland by food supplementing parents with known wintering area. We predicted that experimental chicks (whose parents were supplemented) should have (i) higher growth rates and, (ii) lower ∑OCs due to growth dilution effect and/or due to being fed with less contaminated food compared to control chicks. We also predicted a significant influence of maternal wintering area on chicks' ∑OCs. Plasma ∑OCs of adults, assessed prior to the manipulation, significantly differed between wintering areas of birds. Chicks were weighed every 5 days and plasma ∑OCs were assessed at 20 days old. Based on nitrogen and carbon stable isotope analysis, the supplementary food contributed on average 20% of the dietary protein of the chicks. Although experimental chicks experienced better developmental conditions, supplementary food did not alleviate their organochlorine burden. Nevertheless, chicks whose mothers wintered in Europe showed ∑OCs 50% higher than chicks whose mothers wintered in Africa. Moreover, based on the positive relationship between ∑OCs of chicks and females, the contaminant load of Great skua chicks in Shetland appears to be more influenced by maternal transfer than by trophic transfer.

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.

Perfluoroalkyl substances in eggs and plasma of an avian top predator, great skua (Stercorarius skua), in the North Atlantic.

Temporal, biological, and environmental factors affecting accumulation of perfluoroalkyl substances (PFASs) are poorly understood in comparison with legacy lipid-soluble persistent organic pollutants. Temporal and biological comparisons of PFAS concentrations were made in great skuas (Stercorarius skua), a marine apex predator. Concentrations of 16 PFASs were quantified, including C4-C10 perfluorosulfonates (PFSAs), perfluorooctanesulfonamide (PFOSA), and C5-C14 perfluorocarboxylates (PFCAs). Concentrations of PFASs (ng/g wet wt) were significantly higher in eggs collected in Shetland in 2008 compared with 1980 for most compounds. However, the magnitude of the differences was small, with a mean increase of 3 ng/g. Levels of PFASs in great skuas were low compared with those of other seabirds in similar ecological niches; and in contrast to other contaminants measured in the same eggs, concentrations of PFASs did not correlate with trophic level. Concentrations of PFASs in adult plasma were significantly higher in males than in females for most PFASs. This suggests that maternal transfer through egg laying may be a significant mode of elimination of PFASs in female great skuas. The low concentrations of PFASs in eggs and plasma compared with other halogenated organic contaminants and other species suggest that great skuas do not bioaccumulate PFASs to the same extent as some other seabirds.

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.