Mercury (Hg) is a global contaminant that biomagnifies in marine food webs. Seabirds can serve as valuable bioindicators of marine Hg pollution due to their high trophic positions and broad distributions. However, the biological and spatial drivers of variation in seabird Hg levels remain unclear, and few studies have validated whether seabird-derived estimates of the spatial distribution of Hg are consistent with predictions from biogeochemical-ocean models. We conducted a global meta-analysis of total Hg (THg) concentrations in adult seabird blood. Based on our own fieldwork and a literature review, we compiled 478 mean THg values from 108 species representing >11,000 individuals. Blood THg increased in species feeding at higher trophic levels, with larger body mass, and those more likely to consume mesopelagic prey in oceanic waters. Additionally, blood THg might further increase in regions with low chlorophyll-a level, likely due to greater methylmercury uptake in areas with low-productivity. We subsequently developed models to predict global spatial variation in seabird blood THg, either from all species or only epipelagic prey feeders. Only our epipelagic prey feeder-based model showed a weak significant positive correlation with THg in particulate organic matter from biogeochemical-ocean models. However, the low correlation coefficient (r = 0.23) indicates potential discrepancies between the two models. We suggest that future studies adopt our integrative approach, combining biological data and large-scale modeling, to improve our understanding of global marine Hg pollution. Together, these findings clarify the biological and environmental drivers of Hg exposure in seabirds and highlight the value of seabirds for global monitoring of marine Hg pollution.

Balancing current reproductive investment with survival and future fecundity is a central challenge for long-lived animals, shaping life-history evolution. Although carry-over effects are well documented, the underlying energetic mechanisms remain unclear. Herein, we introduce the energetic flexibility concept, i.e. the ability of individuals to dynamically reallocate energy among competing life-history functions, which serves as a hidden axis influencing carry-over effects. We manipulated energetic costs in breeding black-legged kittiwakes (Rissa tridactyla) through food supplementation and wing-clipping and tracked post-breeding migration. Individuals incurring higher energetic costs exhibited lower immediate breeding success, departed the colony earlier, travelled longer distances, and achieved higher subsequent reproductive success, albeit with reduced apparent survival. Reduced energetic costs did not exhibit detectable carry-over effects on migration or reproduction. Oxidative stress, a proxy for physiological condition, did not increase in individuals with elevated energetic costs, implying prioritized self-maintenance. Collectively, these results showed that individuals flexibly reallocated energy to compensate for short-term costs and invested in future fitness. Our findings provide rare experimental evidence that energetic trade-offs mediate behavioural and reproductive carry-over effects. Recognizing energetic flexibility as a hidden axis of carry-over effects offers a unifying framework for understanding the mechanisms whereby animals balance reproduction, survival and migration in variable environments.

The major histocompatibility complex (MHC) is a gene cluster essential for pathogen recognition in jawed vertebrates. It encompasses the MHC class I genes which primarily recognize intracellular parasites, and the MHC class II genes which primarily recognize extracellular parasites. In wild birds, most studies investigating associations between MHC variants and parasites have been carried out in passerines, and have repeatedly shown that specific MHC class I variants provide resistance to intracellular haemosporidian parasites. In contrast, research on the associations between MHC variants and parasites in non-passerine birds remains limited. In this study, we examined the association between MHC-IIB supertypes and the bacterial load of a sexually transmitted bacterium (named C34) in the black-legged kittiwake (Rissa tridactyla), a genetically monogamous seabird. We focused on MHC class II genes because extracellular parasites are particularly prevalent in non-passerines and may therefore exert strong selection on the studied host. We found that females with lower C34 load had better reproductive performance, and higher probability to carry the MHC-IIB supertype SUP6. In contrast, in males, we observed a positive association between C34 load and reproductive performance, but no association between C34 load and MHC-IIB supertypes. While sexually transmitted diseases are not expected to be a strong selective force in genetically monogamous species, our study suggests that C34 might exert a selective pressure on the evolution of the MHC-IIB. Therefore, further research should explore the influence of sexually transmitted diseases on the reproductive biology of genetically monogamous species.

Animal telemetry is maturing into a viable method for observing the ocean as it can be used to monitor both environmental conditions and biological metrics along the movement trajectories of marine animals. As part of the Cormorant Oceanography Project, we have augmented a biologging tag with an external fast response temperature sensor to collect ocean temperature profiles from the backs of foraging marine birds. Cormorants dive between 50 and 250+ times a day to forage for prey so they can provide hard-to-match temporal and spatial coverage of coastal ocean conditions within their foraging areas. We process tag measurements to obtain fundamental oceanographic data (e.g., temperature profiles, bottom soundings, surface current measurements). Together, we have tracked 17 marine bird species (including two Spheniscus penguins spp. and a sea duck), originating from 17 countries and foraging along the edges of all major oceans. Tagged birds’ distribution included 191 MPAs in 26 countries, offering a unique ocean monitoring method to complement more widely used methods.

Among species reproducing sexually, mating strategies represent a major component of individual fitness. The major histocompatibility complex (MHC) is an extremely diverse set of genes responsible for immunological recognition and defence against pathogens. Although dissimilarity between mates at the major histocompatibility complex has been proposed to drive mate choice through increased offspring pathogen resistance, evidence is mixed. In addition, explorations of the role of the major histocompatibility complex in other mating strategies, such as divorce, are rare. We investigated whether dissimilarity at the major histocompatibility complex class IIB is associated with mate choice and divorce probability in the genetically monogamous black-legged kittiwake ( Rissa tridactyla ). We found that first-time male breeders, as well as divorced males, were paired with females more dissimilar at the major histocompatibility complex class IIB than expected under random mating. We did not find evidence for mate choice based on major histocompatibility complex class IIB dissimilarity when considering females. In addition, in the studied population, divorce probability was very low compared with other populations and did not significantly vary with the dissimilarity of the pair at the major histocompatibility complex class IIB. Our results pave the way to a better understanding of the complex role of major histocompatibility complex dissimilarity in mating decisions of species displaying mutual choice and biparental care.

Energy is a common currency for any living organism, yet estimating energy expenditure in wild animals is challenging. Accelerometers are commonly used to estimate energy expenditure, via a dynamic body acceleration (DBA) or time-energy budget approach. The DBA approach estimates energy expenditure directly from acceleration but may lead to erroneous estimates during inactivity when acceleration is zero but energy expenditure is not. The time-energy budget approach uses accelerometers and other data streams to assign a behaviour to each time step, and then calculates energy expenditure based on activity-specific metabolic rates assigned to each behaviour. Here, we used GPS-accelerometry in breeding black-legged kittiwakes (Rissa tridactyla, n=80) to calculate DBA and time-energy budgets derived from simple biologging metrics (speed, wingbeat frequency, GPS position). We then compared these two approaches with estimates of energy expenditure from doubly labelled water (DLW). Energy expenditure estimated from DLW correlated with DBA, but the best model to estimate energy expenditure was based on time-energy budgets. Energetic costs of flapping flight were higher than all other kittiwake behaviours (5.54xbasal metabolic rate, BMR). Energetic costs of gliding flight (0.80xBMR) were the lowest of all behaviours, and equivalent to the cost of resting at the colony. DEE for our birds estimated from our calibration coefficients was similar to DEE for our birds estimated with the model coefficient published using different methods. We conclude that once calibrated with DLW, GPSaccelerometry provides a simple method for measuring energy expenditure in wild kittiwakes based on time-energy budgets.

Among species reproducing sexually, mating strategies represent a major component of individual fitness. The Major Histocompatibility Complex (MHC) is an extremely diverse set of genes responsible for immunological recognition and defense against pathogens. Although MHC-dissimilarity between mates has been proposed to drive mate choice through increased offspring pathogen resistance, evidence is mixed, and evidence for other MHC-based mating strategies remains rare. We investigated whether MHC-IIB dissimilarity is associated with mate choice and mate change in the genetically monogamous black-legged kittiwake (Rissa tridactyla). We found that first-time male breeders are paired with females more MHC-IIB dissimilar to them than expected by chance. After a successful reproduction, the more males are MHC-IIB dissimilar to their mate, the less likely they are to change mate. When males change their mate, they tend to be more MHC-IIB dissimilar to the new mate compared to the previous mate. However, males are not more MHC-IIB dissimilar to their new mate than expected by chance. We did not find evidence for an effect of MHC-IIB dissimilarity on mating strategies when considering the female's perspective. Male mate choice should not be overlooked in species with bi-parental care in which the male performs a significant part of parental care. ### Competing Interest Statement The authors have declared no competing interest.

Investigator disturbance while monitoring seabirds can result in lower survival rates and breeding success, leaving lasting negative impacts on the population and biasing observations. For example, monitoring rhinoceros auklets ( Cerorhinca monocerata ) and other burrowing alcids can reduce breeding success or even survival through handling stress and damage to nesting habitat. For this reason, researchers must seek to decrease colony disturbance. Automated radio-frequency identification (RFID) via passive integrated transponder (PIT) tags is an inexpensive and reliable way to identify individual presence and record attendance behaviour, avoiding the need to recapture seabirds or visit the colony frequently. PIT tags either can be implanted subcutaneously or attached externally to leg bands, but it is unclear which method causes lower disturbance. To examine the impact of PIT tagging on rhinoceros auklets nesting in artificial burrows on Middleton Island, Alaska, we monitored burrow entrances with automated recording RFID readers to collect presence and nest attendance data. PIT-tagged (either band attachment or subcutaneous implant) and control birds had similar breeding success and chick growth rates. Breeding success was similar between nests with one or two parents marked. Birds tagged externally were detected less often than birds marked with a subcutaneous implant. We conclude that PIT tagging of rhinoceros auklets is a relatively non-invasive method for seabird monitoring, and that subcutaneous implants do not cause more disturbance than external attachment.

Mercury (Hg) is a metallic trace element toxic for humans and wildlife that can originate from natural and anthropic sources. Hg spatial gradients have been found in seabirds from the Arctic and other oceans, suggesting contrasting toxicity risks across regions. Selenium (Se) plays a protective role against Hg toxicity, but its spatial distribution has been much less investigated than that of Hg. From 2015 to 2017, we measured spatial co-exposure of Hg and Se in blood samples of two seabird species, the Brünnich's guillemot (Uria lomvia) and the black-legged kittiwake (Rissa tridactyla) from 17 colonies in the Arctic and subarctic regions, and we calculated their molar ratios (Se:Hg), as a measure of Hg sequestration by Se and, therefore, of Hg exposure risk. We also evaluated concentration differences between species and ocean basins (Pacific-Arctic and Atlantic-Arctic), and examined the influence of trophic ecology on Hg and Se concentrations using nitrogen and carbon stable isotopes. In the Atlantic-Arctic ocean, we found a negative west-to-east gradient of Hg and Se for guillemots, and a positive west-to-east gradient of Se for kittiwakes, suggesting that these species are better protected from Hg toxicity in the European Arctic. Differences in Se gradients between species suggest that they do not follow environmental Se spatial variations. This, together with the absence of a general pattern for isotopes influence on trace element concentrations, could be due to foraging ecology differences between species. In both oceans, the two species showed similar Hg concentrations, but guillemots showed lower Se concentrations and Se:Hg than kittiwakes, suggesting a higher Hg toxicity risk in guillemots. Within species, neither Hg, nor Se or Se:Hg differed between both oceans. Our study highlights the importance of considering Se together with Hg, along with different species and regions, when evaluating Hg toxic effects on marine predators in international monitoring programs.

We provide evidence of anthropogenic materials ingestion in seabirds from a remote oceanic area, using regurgitates obtained from black-legged kittiwake (Rissa tridactyla) chicks from Middleton Island (Gulf of Alaska, USA). By means of GPS tracking of breeding adults, we identified foraging grounds where anthropogenic materials were most likely ingested. They were mainly located within the continental shelf of the Gulf of Alaska and near the Alaskan coastline. Anthropogenic cellulose fibers showed a high prevalence (85 % occurrence), whereas synthetic polymers (in the micro- and mesoplastics dimensional range) were less frequent (20 %). Most fibers (60 %) were blue and we confirmed the presence of indigo-dyed cellulosic fibers, characteristic of denim fabrics. In terms of mass, contamination levels were 0.077 μg g-1 wet weight and 0.009 μg g-1 wet weight for anthropogenic microfibers and synthetic polymers, respectively. These results represent the only recent report of contamination by anthropogenic fibers in seabirds from the Gulf of Alaska.

Repeated use of a winning foraging strategy can be profitable when individuals use memory to return to successful food patches. However, in environments where patches are unpredictable, variable foraging behaviour may be more profitable. To test this idea, we explored how individual variation in foraging trip characteristics impacts breeding success in black-legged kittiwakes, Rissa tridactyla, on Middleton Island, Alaska, U.S.A., during a period of highly variable environmental conditions, the largest recorded marine heatwave. As anticipated, foraging trip characteristics were highly variable, within and between years and individuals. While characteristics of foraging trips alone did not influence annual breeding success, both age and variance in those trip characteristics explained variation in breeding success. Specifically, individuals with smaller variance in foraging trip characteristics among trips were more likely to fledge a chick. There was a maximum distance threshold in foraging implying that individuals searched within a restricted area, increasing foraging time rather than distance when searching was not profitable, and providing additional support for the idea that kittiwakes are most successful when foraging in known areas rather than exploring new areas. The Pacific Decadal Oscillation, which is associated with large scale shifts between cold and warm ocean climate and ecosystem regimes in the region, impacted breeding success but did not change foraging behaviour. However, mean breeding success decreased as mean time spent resting and in area-restricted search (intensive search) on foraging trips during incubation increased. Based on nearly a decade of data, we conclude that smaller variability in behaviour, even during challenging foraging conditions, enhances breeding success. As climate change and marine heatwaves continue to increase in intensity, individuals more variable in foraging behaviour may be unable to compensate.

Although the effect of sperm quality is well studied in the context of sperm competition, its effect on offspring performance, especially after the embryo stages, has been less investigated. Here, we investigated whether the proportion of spermatozoa with normal morphology was associated with offspring performance during chick development in the black-legged kittiwake, a behaviorally and genetically monogamous seabird in which sperm competition is absent. First, we found that, at hatching, the difference in body condition between the first- and second-hatched siblings was higher when the father had a lower proportion of normal spermatozoa. We discuss this result in light of maternal allocation strategy to manipulate sibling competition. Second, we showed that, in first-hatched chicks, body mass growth between hatching and the age of 10 days, body condition at the age of 10 days and maximum body mass reached before fledging were positively related to the proportion of normal spermatozoa in the father’s sperm. Overall, our results support the role of sperm quality on offspring performance in the black-legged kittiwake and call for further studies investigating the importance of sperm quality in genetically monogamous species. The importance of sperm quality has been poorly studied in other contexts than sperm competition. We show that, in a genetically monogamous seabird, the mass growth and condition of first-hatched chicks increase with the proportion of normal spermatozoa in the father’s sperm. Unexpectedly, our results further suggest that females might differentially invest into eggs according to traits correlated with the quality of their partner’s sperm.

Abstract Life‐history theory predicts that investment in reproduction should decrease survival (the ‘cost of reproduction’). It is often assumed that energy allocation drives such trade‐offs, with limited energy available for both reproduction and survival. However, the underlying mechanisms remain poorly understood, maybe because survival costs of reproduction are only apparent when resources are limited. Here, we took advantage of a natural experiment created by fluctuating environmental conditions to compare energy expenditure of a seabird, the pelagic cormorant (Phalacrocorax pelagicus), between contrasting population‐scale scenarios of survival costs of reproduction. We used multi‐state capture–recapture modelling across 16 years to identify which breeding seasons induced high survival costs (survival ratebreeders < survival ratenon/failed breeders) and we concomitantly estimated energy expenditure of chick‐rearing males using time‐energy budget models across 4 years. Daily energy expenditure (DEE) of chick‐rearing pelagic cormorants varied significantly among years. However, survival costs of reproduction were observed in only 1 year, and contrary to our expectations, variation in DEE was not associated with population‐level survival costs. Similarly, at the individual level, DEE in 1 year did not predict the probability of being observed again at the colony in following years (apparent survival). Finally, DEE was independent of brood size and brood age, but older individuals tended to expend less energy than younger ones. Given the lack of an apparent energetic ‘cost of reproduction’, lower DEE in older birds could be due to improved efficiency rather than avoidance of costs in old birds. Although future studies should account for potential sex‐specific energetic constraints by including data on female energy expenditure, we conclude that a direct link between the rate of energy expenditure during breeding and subsequent survival is unlikely in this system.

Because of ongoing rapid climate change, many ecosystems are becoming both warmer and more variable, and these changes are likely to alter the magnitude and variability of natural selection acting on wild populations. Critically, changes and fluctuations in selection can impact both population demography and evolutionary change. Therefore, predicting the impacts of climate change depends on understanding the magnitude and variation in selection on traits across different life stages and environments. Long-term experiments in wild settings are a great opportunity to determine the impact of environmental conditions on selection. Here we examined variability in the strength of selection on size traits of nestling black-legged kittiwakes (Rissa tridactyla) in a 25-year study including a food supplementation experiment on Middleton Island in the Gulf of Alaska. Using mixed effect models, we examined the annual variability of stage-specific and resource-specific selection gradients across 25 years. We found that (a) larger and heavier hatchlings were the most likely to survive during early ontogeny, (b) non-food supplemented younger nestlings in a brood experienced the strongest selection, and (c) warmer conditions increased the magnitude of selection on nestling mass and affected non-food supplemented and second-hatched nestlings the most. Our results suggested that variable resource dynamics likely caused some of the changes in selection from year to year and that warming conditions increased the strength of selection on subarctic seabird growth. However, our experimental manipulation revealed that local environmental heterogeneity could buffer the selection expected from broader climatic changes. Consequently, understanding the interactive effects of local conditions and general changes in climate seems likely to improve our ability to predict future selection gradients.

Climate change is altering species' traits across the globe. To predict future trait changes and understand the consequences of those changes, we need to know the environmental drivers of phenotypic change. In the present study, we use multi‐decadal long datasets to determine periods of within‐year environmental variation that predict growth of three seabird species. We evaluate whether these periods changed over time and use them to predict future growth under climate change. We find that predictions of trait change could be improved by considering that 1) the timing of environmental factors used to predict traits (predictive‐environmental features) can change over time, and 2) the type of predictive‐environmental features can change over time. We find evidence of changes in the timing of environmental predictors in all populations studied and evidence for a change in the type of predictor in the studied Arctic murre population. Environmental models of growth predict that warming conditions will decrease growth rates and bird body sizes in two species (black‐legged kittiwake Rissa tridactyla and glaucous‐winged gull Larus Larus glaucescens), but not the third (thick‐billed murre Uria lomvia). Consequently, climate change is likely to decrease fledging rates in the gulls and kittiwakes. Further, we find that sea ice‐cover historically predicted murre chick growth well, but no longer does – instead air temperature is now a better predictor of murre growth. Our study highlights a need to investigate whether environmental determinants of trait variation commonly shift in a changing climate and whether such changes have implications for adaptation to novel environments.

The ability to efficiently measure the health and nutritional status of wild populations in situ is a valuable tool, as many methods of evaluating animal physiology do not occur in real-time, limiting the possibilities for direct intervention. This study investigates the use of blood plasma metabolite concentrations, measured via point-of care devices or a simple plate reader assay, as indicators of nutritional state in free-living seabirds. We experimentally manipulated the energy expenditure of wild black-legged kittiwakes on Middleton Island, Alaska, and measured the plasma concentrations of glucose, cholesterol, B-hydroxybutyrate, and triglycerides throughout the breeding season, along with measures of body condition (size-corrected mass [SCM] and muscle depth). Supplemental feeding improved the nutritional state of kittiwakes by increasing feeding rate (higher glucose and triglycerides, lower cholesterol), and flight-handicapping caused a slight nutritional decline (lower glucose and triglycerides, higher cholesterol and B-hydroxybutyrate). Glucose and triglycerides were the best indicators of nutritional state when used alongside SCM, and improved upon commonly used metrics for measuring individual condition (i.e. SCM or mass alone). Metabolite concentrations varied across the breeding period, suggesting that the pre-laying stage, when feeding rates tend to be lower, was the most nutritionally challenging period for kittiwakes (low glucose, high cholesterol). Muscle depth also varied by treatment and breeding stage, but differed from other nutritional indices, suggesting that muscle depth is an indicator of exercise and activity level rather than nutrition. Here we demonstrate potential for the use of blood plasma metabolites measured via point of-care devices as proxies for evaluating individual health, population health, and environmental food availability.

Amidst the current biodiversity crisis, the availability of genomic resources for declining species can provide important insights into the factors driving population decline. In the early 1990s, the black-legged kittiwake (Rissa tridactyla), a pelagic gull widely distributed across the arctic, subarctic, and temperate zones, suffered a steep population decline following an abrupt warming of sea surface temperature across its distribution range and is currently listed as Vulnerable by the International Union for the Conservation of Nature. Kittiwakes have long been the focus for field studies of physiology, ecology, and ecotoxicology and are primary indicators of fluctuating ecological conditions in arctic and subarctic marine ecosystems. We present a high-quality chromosome-level reference genome and annotation for the black-legged kittiwake using a combination of Pacific Biosciences HiFi sequencing, Bionano optical maps, Hi-C reads, and RNA-Seq data. The final assembly spans 1.35 Gb across 32 chromosomes, with a scaffold N50 of 88.21 Mb and a BUSCO completeness of 97.4%. This genome assembly substantially improves the quality of a previous draft genome, showing an approximately 5x increase in contiguity and a more complete annotation. Using this new chromosome-level reference genome and three more chromosome-level assemblies of Charadriiformes, we uncover several lineage-specific chromosome fusions and fissions, but find no shared rearrangements, suggesting that interchromosomal rearrangements have been commonplace throughout the diversification of Charadriiformes. This new high-quality genome assembly will enable population genomic, transcriptomic, and phenotype-genotype association studies in a widely studied sentinel species, which may provide important insights into the impacts of global change on marine systems.

Multi-colony studies of breeding seabirds may provide insights into the mechanistic links between large-scale climate variability and local changes in prey availability. In the North Pacific, the Pacific Decadal Oscillation (PDO) is a dominant climate index characterized by contrasting patterns in sea surface temperature between the western and eastern North Pacific. To examine how inter-annual variability in the PDO affects rhinoceros auklets Cerorhinca monocerata across the North Pacific, we measured inter-annual changes in nutritional stress (as reflected in plasma levels of corticosterone) of adults breeding on 5 colonies (2 and 3 colonies from the western and eastern Pacific, respectively). We also examined concurrent changes in mass and energy content of food loads delivered to chicks. We found that higher summer PDO values were associated with increased corticosterone levels and lower mass and energy contents of the food loads in both the western and eastern North Pacific colonies. Results indicated that oceanographic conditions during higher PDO values induced local changes in forage fish communities, leading to reduced prey availability, which, in turn, increased the nutritional stress of breeding birds. We conclude that the higher summer PDO index in recent years was associated with food-poor conditions for breeding rhinoceros auklets across their reproductive range, and prolonged periods of high summer PDO may be detrimental to the populations of this seabird species. Our results highlight the complexity of the mechanisms of how large-scale climate variability affects seabirds with a large geographical distribution.