Raising offspring increases ageing: Differences in senescence among three populations of a long-lived seabird, the Atlantic puffin.

Actuarial senescence, the decline of survival with age, is well documented in the wild. Rates of senescence vary widely between taxa, to some extent also between sexes, with the fastest life histories showing the highest rates of senescence. Few studies have investigated differences in senescence among populations of the same species, although such variation is expected from population-level differences in environmental conditions, leading to differences in vital rates and thus life histories. We predict that, within species, populations differing in productivity (suggesting different paces of life) should experience different rates of senescence, but with little or no sexual difference in senescence within populations of monogamous, monomorphic species where the sexes share breeding duties. We compared rates of actuarial senescence among three contrasting populations of the Atlantic puffin Fratercula arctica. The dataset comprised 31 years (1990-2020) of parallel capture-mark-recapture data from three breeding colonies, Isle of May (North Sea), Røst (Norwegian Sea) and Hornøya (Barents Sea), showing contrasting productivities (i.e. annual breeding success) and population trends. We used time elapsed since first capture as a proxy for bird age, and productivity and the winter North Atlantic Oscillation Index (wNAO) as proxies for the environmental conditions experienced by the populations within and outside the breeding season, respectively. In accordance with our predictions, we found that senescence rates differed among the study populations, with no evidence for sexual differences. There was no evidence for an effect of wNAO, but the population with the lowest productivity, Røst, showed the lowest rate of senescence. As a consequence, the negative effect of senescence on the population growth rate (λ) was up to 3-5 times smaller on Røst (Δλ = -0.009) than on the two other colonies. Our findings suggest that environmentally induced differences in senescence rates among populations of a species should be accounted for when predicting effects of climate variation and change on species persistence. There is thus a need for more detailed information on how both actuarial and reproductive senescence influence vital rates of populations of the same species, calling for large-scale comparative studies.

Earlier colony arrival but no trend in hatching timing in two congeneric seabirds (Uria spp.) across the North Atlantic.

A global analysis recently showed that seabird breeding phenology (as the timing of egg-laying and hatching) does not, on average, respond to temperature changes or advance with time (Keogan et al. 2018 Nat. Clim. Change8, 313-318). This group, the most threatened of all birds, is therefore prone to spatio-temporal mismatches with their food resources. Yet, other aspects of the breeding phenology may also have a marked influence on breeding success, such as the arrival date of adults at the breeding site following winter migration. Here, we used a large tracking dataset of two congeneric seabirds breeding in 14 colonies across 18° latitudes, to show that arrival date at the colony was highly variable between colonies and species (ranging 80 days) and advanced 1.4 days/year while timing of egg-laying remained unchanged, resulting in an increasing pre-laying duration between 2009 and 2018. Thus, we demonstrate that potentially not all components of seabird breeding phenology are insensitive to changing environmental conditions.

Blood plasma clinical-chemical parameters as biomarker endpoints for organohalogen contaminant exposure in Norwegian raptor nestlings.

Raptors are exposed to biomagnifying and toxic organohalogenated compounds (OHCs) such as organochlorines, brominated flame retardants and perfluorinated compounds. To investigate how OHC exposure may affect biochemical pathways we collected blood plasma from Norwegian northern goshawk (n=56), golden eagle (n=12) and white-tailed eagle (n=36) nestlings during three consecutive breeding seasons. We found that blood plasma concentrations of calcium, sodium, creatinine, cholesterol, albumin, total protein, urea, inorganic phosphate, protein:creatinine, urea:creatinine and uric acid:creatinine ratios and liver enzymes ALKP and ALAT were positively correlated to PCBs, chlordanes, p,p'-DDE, HCB, PFCs and/or PBDEs. Total bilirubin and glucose were negatively correlated to PCBs while magnesium and potassium were negatively correlated to HCB and p,p'-DDE. In addition, protein:creatinine and ALAT were also negatively correlated to PCBs and PFCs, respectively. The most significant relationships were found for the highly contaminated northern goshawks and white-tailed eagles. The statistical relationships between OHCs and BCCPs indicate that biochemical pathways could be influenced while it is uncertain if such changes have any health effects. The OHC concentrations were below concentrations causing reproductive toxicity in adults of other raptor species but similar to those of concern for endocrine disruption of thyroid hormones in e.g., bald eagles.

Complex population structure of the Atlantic puffin revealed by whole genome analyses.

The factors underlying gene flow and genomic population structure in vagile seabirds are notoriously difficult to understand due to their complex ecology with diverse dispersal barriers and extensive periods at sea. Yet, such understanding is vital for conservation management of seabirds that are globally declining at alarming rates. Here, we elucidate the population structure of the Atlantic puffin (Fratercula arctica) by assembling its reference genome and analyzing genome-wide resequencing data of 72 individuals from 12 colonies. We identify four large, genetically distinct clusters, observe isolation-by-distance between colonies within these clusters, and obtain evidence for a secondary contact zone. These observations disagree with the current taxonomy, and show that a complex set of contemporary biotic factors impede gene flow over different spatial scales. Our results highlight the power of whole genome data to reveal unexpected population structure in vagile marine seabirds and its value for seabird taxonomy, evolution and conservation.

Perfluorinated, brominated, and chlorinated contaminants in a population of lesser black-backed gulls (Larus fuscus).

Protein-bound perfluorinated compounds (PFCs) and lipid-soluble polybrominated diphenyl ethers (PBDEs) and organochlorines (OCs) were measured in whole blood from a large number (n = 83) of breeding lesser black-backed gulls (Larus fuscus) caught during two distinct sampling periods in a colony on the coast of northern Norway. We analyzed 14 PFCs (seven were detected in more than 75% of samples), 10 PBDEs (only BDE 47 was detected), and 27 OCs, including 12 polychlorinated biphenyl (PCB) congeners (14 OCs were detected). Median total PFC concentration was higher than median total OC concentration (43 vs 39 ng/g wet wt). Perfluorooctane sulfonate (PFOS) was the dominant PFC (mean relative contribution of PFOS to total contaminant concentration in blood [Sigmatotal contaminants] was 38%), whereas total PCB (26% of Sigmatotal contaminants) and p,p'-DDE (2,2-bis(4-chlorophenyl)-1,1-dichloroethene; 13% of Sigmatotal contaminants) were the dominant OCs. No covariability was found between protein-bound and lipid-soluble compounds; individuals with high concentrations of PFCs did not have high concentrations of OCs or BDE 47. The concentrations of PFCs were lower in birds caught during the late sampling period compared to those of the early period, and females had lower levels of some PFCs compared with males, suggesting that females sequester fluorinated substances into eggs. For lipid-soluble compounds, no significant sex or sampling period differences were found, except that trans-nonachlor, cis-nonachlor, and p,p'-DDE concentrations were lower in birds caught during the late sampling period. The pattern of PFC compounds (relative to PFOS) and lipid-soluble compounds (relative to PCB 153) differed between sampling periods in females but not in males. Finally, PFCs were distributed more uniformly within the population than the lipid-soluble compounds, for which the distributions were strongly negatively skewed.

Ocean-wide Drivers of Migration Strategies and Their Influence on Population Breeding Performance in a Declining Seabird.

Which factors shape animals' migration movements across large geographical scales, how different migratory strategies emerge between populations, and how these may affect population dynamics are central questions in the field of animal migration [1] that only large-scale studies of migration patterns across a species' range can answer [2]. To address these questions, we track the migration of 270 Atlantic puffins Fratercula arctica, a red-listed, declining seabird, across their entire breeding range. We investigate the role of demographic, geographical, and environmental variables in driving spatial and behavioral differences on an ocean-basin scale by measuring puffins' among-colony differences in migratory routes and day-to-day behavior (estimated with individual daily activity budgets and energy expenditure). We show that competition and local winter resource availability are important drivers of migratory movements, with birds from larger colonies or with poorer local winter conditions migrating further and visiting less-productive waters; this in turn led to differences in flight activity and energy expenditure. Other behavioral differences emerge with latitude, with foraging effort and energy expenditure increasing when birds winter further north in colder waters. Importantly, these ocean-wide migration patterns can ultimately be linked with breeding performance: colony productivity is negatively associated with wintering latitude, population size, and migration distance, which demonstrates the cost of competition and migration on future breeding and the link between non-breeding and breeding periods. Our results help us to understand the drivers of animal migration and have important implications for population dynamics and the conservation of migratory species.

Anti-parasite treatment removes negative effects of environmental pollutants on reproduction in an Arctic seabird.

Recent studies have shown that the detrimental effects of anthropogenic pollutants may be worse if organisms are exposed to natural stress. In this study, we examined whether negative effects of organochlorines (OCs) could be influenced by parasites. In two breeding seasons, we administered an anti-helminthic drug to groups of breeding glaucous gulls (Larus hyperboreus), whereas control groups were placebo treated. In all birds, blood residues of the most important OCs in the study population (hexachlorobenzene, oxychlordane, p,p'-dichlorodiphenyldichloroethylene and polychlorinated biphenyl), were measured. The relationships between OCs and fitness components (i.e. nesting success and return rate between breeding seasons) were then compared between the birds receiving anti-parasite treatment and the controls. Among untreated males, higher blood residues of OCs were associated with lowered nesting success, while in males receiving anti-parasite treatment, there was no detrimental effect of OCs on fitness. Return rate was not affected by treatment or OCs. Our findings suggest that parasites may be an important factor in triggering reproductive effects of such pollutants, and that relatively low levels of OCs may have serious reproductive consequences in natural populations when stress from other sources is high.

The stress hormone corticosterone in a marine top predator reflects short-term changes in food availability.

In many seabird studies, single annual proxies of prey abundance have been used to explain variability in breeding performance, but much more important is probably the timing of prey availability relative to the breeding season when energy demand is at a maximum. Until now, intraseasonal variation in prey availability has been difficult to quantify in seabirds. Using a state-of-the-art ocean drift model of larval cod Gadus morhua, an important constituent of the diet of common guillemots Uria aalge in the southwestern Barents Sea, we were able to show clear, short-term correlations between food availability and measurements of the stress hormone corticosterone (CORT) in parental guillemots over a 3-year period (2009-2011). The model allowed the extraction of abundance and size of cod larvae with very high spatial (4 km) and temporal resolutions (1 day) and showed that cod larvae from adjacent northern spawning grounds in Norway were always available near the guillemot breeding colony while those from more distant southerly spawning grounds were less frequent, but larger. The latter arrived in waves whose magnitude and timing, and thus overlap with the guillemot breeding season, varied between years. CORT levels in adult guillemots were lower in birds caught after a week with high frequencies of southern cod larvae. This pattern was restricted to the two years (2009 and 2010) in which southern larvae arrived before the end of the guillemot breeding season. Any such pattern was masked in 2011 by already exceptionally high numbers of cod larvae in the region throughout chick-rearing period. The findings suggest that CORT levels in breeding birds increase when the arrival of southern sizable larvae does not match the period of peak energy requirements during breeding.

Climate-driven ichthyoplankton drift model predicts growth of top predator young.

Climate variability influences seabird population dynamics in several ways including access to prey near colonies during the critical chick-rearing period. This study addresses breeding success in a Barents Sea colony of common guillemots Uria aalge where trophic conditions vary according to changes in the northward transport of warm Atlantic Water. A drift model was used to simulate interannual variations in transport of cod Gadus morhua larvae along the Norwegian coast towards their nursery grounds in the Barents Sea. The results showed that the arrival of cod larvae from southern spawning grounds had a major effect on the size of common guillemot chicks at fledging. Furthermore, the fraction of larvae from the south was positively correlated to the inflow of Atlantic Water into the Barents Sea thus clearly demonstrating the mechanisms by which climate-driven bottom-up processes influence interannual variations in reproductive success in a marine top predator.

Plasma concentrations of organohalogenated pollutants in predatory bird nestlings: associations to growth rate and dietary tracers.

The extent to which persistent organic pollutants (POPs) with different physicochemical properties originated from the food (dietary input) was assessed in raptor nestlings. Lipophilic polychlorinated biphenyl (PCB) 153, 1-dichloro-2,2-bis(p-chlorophenyl)ethylene (p,p'-DDE), and hexachlorobenzene (HCB), and protein-bound perfluorooctane sulfonate (PFOS), were measured repeatedly in blood plasma of individual goshawk (Accipiter gentilis) and white-tailed eagle (Haliaeetus albicilla) nestlings, 1 to 3 wk after hatching and near fledging. Maternally derived POPs dilute as nestlings grow (growth dilution), and increasing plasma concentrations would indicate dietary input. First, plasma concentrations given no dietary input were estimated, and concentrations of p,p'-DDE, HCB, and notably PFOS were significantly higher than predicted from a growth-dilution scenario (approximately 1.5-fold to 2.5-fold higher; p < 0.001). In contrast, PCB 153 declined in both species, although concentrations were still higher than predicted in white-tailed eagle nestlings (p < 0.05). Second, the relationships between plasma POP concentrations and trophic position (δ(15) N) and dietary carbon source (δ(13) C) were analyzed, controlling for growth rate. Both δ(15) N and δ(13) C (measured in body feathers) were significantly associated to the accumulation of most POPs, except PFOS. In conclusion, pollutant data acquired in plasma of nestling raptors should be interpreted and further investigated in the light of individual feeding ecology, and the use of raptor nestlings as sentinels for POP monitoring could be optimized by correcting for different factors such as body condition, brood size, and age.

Ecological and spatial factors drive intra- and interspecific variation in exposure of subarctic predatory bird nestlings to persistent organic pollutants.

Top predators in northern ecosystems may suffer from exposure to persistent organic pollutants (POPs) as this exposure may synergistically interact with already elevated natural stress in these ecosystems. In the present study, we aimed at identifying biological (sex, body condition), ecological (dietary carbon source, trophic level) and spatial factors (local habitat, regional nest location) that may influence intra- and interspecific variation in exposure of subarctic predatory bird nestlings to polychlorinated biphenyl 153 (CB 153), polybrominated diphenyl ether 47 (BDE 47), dichlorodiphenyldichloroethylene (p,p'-DDE) and hexachlorobenzene (HCB). During three breeding seasons (2008-2010), we sampled body feathers from fully-grown nestlings of three ecologically distinct predatory bird species in subarctic Norway: Northern Goshawk (Accipiter gentilis), White-tailed Eagle (Haliaeetus albicilla) and Golden Eagle (Aquila chrysaetos). The present study analysed, for the first time, body feathers for both POPs and carbon (δ(13)C) and nitrogen (δ(15)N) stable isotopes, thus integrating the dietary carbon source, trophic level and POP exposure for the larger part of the nestling stage. Intraspecific variation in exposure was driven by a combination of ecological and spatial factors, often different for individual compounds. In addition, combinations for individual compounds differed among species. Trophic level and local habitat were the predominant predictors for CB 153, p,p'-DDE and BDE 47, indicating their biomagnification and decreasing levels according to coast>fjord>inland. Variation in exposure may also have been driven by inter-annual variation arisen from primary sources (e.g. p,p'-DDE) and/or possible revolatilisation from secondary sources (e.g. HCB). Interspecific differences in POP exposure were best explained by a combination of trophic level (biomagnification), dietary carbon source (food chain discrimination) and regional nest location (historical POP contamination). In conclusion, the combined analysis of POPs and stable isotopes in body feathers from fully-grown nestlings has identified ecological and spatial factors that may drive POP exposure over the larger part of the nestling stage. This methodological approach further promotes the promising use of nestling predatory bird body feathers as a non-destructive sampling strategy to integrate various toxicological and ecological proxies.

A label of health: a previous immune challenge is reflected in the expression of a female plumage trait.

Studies of ornaments as indicators of individual quality have hitherto focused on males, while studies of female ornaments have been almost absent. However, females within the same species may show large variation in both outer appearance and individual quality. We experimentally examined the effect of an immune challenge on the size of white fringes in the wing feathers produced one to two months after the challenge in female common eiders (Somateria mollissima), a long-lived sea duck. Immune-challenged females produced feathers with smaller white fringes, showing that a previous immune challenge may affect the expression of a plumage trait. We also report an unexpected difference in the expression of this white plumage trait within the immune-challenged group, related to the specific immune response against one of the injected antigens.