Seabirds reveal mercury distribution across the North Atlantic.

Mercury (Hg) is a heterogeneously distributed toxicant affecting wildlife and human health. Yet, the spatial distribution of Hg remains poorly documented, especially in food webs, even though this knowledge is essential to assess large-scale risk of toxicity for the biota and human populations. Here, we used seabirds to assess, at an unprecedented population and geographic magnitude and high resolution, the spatial distribution of Hg in North Atlantic marine food webs. To this end, we combined tracking data of 837 seabirds from seven different species and 27 breeding colonies located across the North Atlantic and Atlantic Arctic together with Hg analyses in feathers representing individual seabird contamination based on their winter distribution. Our results highlight an east-west gradient in Hg concentrations with hot spots around southern Greenland and the east coast of Canada and a cold spot in the Barents and Kara Seas. We hypothesize that those gradients are influenced by eastern (Norwegian Atlantic Current and West Spitsbergen Current) and western (East Greenland Current) oceanic currents and melting of the Greenland Ice Sheet. By tracking spatial Hg contamination in marine ecosystems and through the identification of areas at risk of Hg toxicity, this study provides essential knowledge for international decisions about where the regulation of pollutants should be prioritized.

Spatial distribution of selenium-mercury in Arctic seabirds.

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.

Lower nutritional state and foraging success in an Arctic seabird despite behaviorally flexible responses to environmental change.

The degree to which individuals adjust foraging behavior in response to environmental variability can impact foraging success, leading to downstream impacts on fitness and population dynamics. We examined the foraging flexibility, average daily energy expenditure, and foraging success of an ice-associated Arctic seabird, the thick-billed murre (Uria lomvia) in response to broad-scale environmental conditions at two different-sized, low Arctic colonies located <300 km apart. First, we compared foraging behavior (measured via GPS units), average daily energy expenditure (estimated from GPS derived activity budgets), and foraging success (nutritional state measured via nutritional biomarkers pre- and post- GPS deployment) of murres at two colonies, which differ greatly in size: 30,000 pairs breed on Coats Island, Nunavut, and 400,000 pairs breed on Digges Island, Nunavut. Second, we tested whether colony size within the same marine ecosystem altered foraging behavior in response to broad-scale environmental variability. Third, we tested whether environmentally induced foraging flexibility influenced the foraging success of murres. Murres at the larger colony foraged farther and longer but made fewer trips, resulting in a lower nutritional state and lower foraging success compared to birds at the smaller colony. Foraging behavior and foraging success varied in response to environmental variation, with murres at both colonies making longer, more distant foraging trips in high ice regimes during incubation, suggesting flexibility in responding to environmental variability. However, only birds at the larger colony showed this same flexibility during chick rearing. Foraging success at both colonies was higher during high ice regimes, suggesting greater prey availability. Overall, murres from the larger colony exhibited lower foraging success, and their foraging behavior showed stronger responses to changes in broad-scale conditions such as sea ice regime. Taken together, this suggests that larger Arctic seabird colonies have higher behavioral and demographic sensitivity to environmental change.

Behavioural flexibility in an Arctic seabird using two distinct marine habitats to survive the energetic constraints of winter.

BACKGROUND: Homeothermic marine animals in Polar Regions face an energetic bottleneck in winter. The challenges of short days and cold temperatures are exacerbated for flying seabirds with small body size and limited fat stores. We use biologging approaches to examine how habitat, weather, and moon illumination influence behaviour and energetics of a marine bird species, thick-billed murres (Uria lomvia). METHODS: We used temperature-depth-light recorders to examine strategies murres use to survive winter in the Northwest Atlantic, where contrasting currents create two distinct marine habitats: cold (-0.1 ± 1.2 °C), shallower water along the Labrador Shelf and warmer (3.1 ± 0.3 °C), deep water in the Labrador Basin. RESULTS: In the cold shelf water, murres used a high-energy strategy, with more flying and less diving each day, resulting in high daily energy expenditure and also high apparent energy intake; this strategy was most evident in early winter when day lengths were shortest. By contrast, murres in warmer basin water employed a low-energy strategy, with less time flying and more time diving under low light conditions (nautical twilight and night). In warmer basin water, murres increased diving at night when the moon was more illuminated, likely taking advantage of diel vertically migrating prey. In warmer basin water, murres dove more at night and foraging efficiency increased under negative North Atlantic Oscillation (calmer ocean conditions). CONCLUSIONS: The proximity of two distinct marine habitats in this region allows individuals from a single species to use dual (low-energy/high-energy) strategies to overcome winter energy bottlenecks.

Foraging range scales with colony size in high-latitude seabirds.

Density-dependent prey depletion around breeding colonies has long been considered an important factor controlling the population dynamics of colonial animals.1-4 Ashmole proposed that as seabird colony size increases, intraspecific competition leads to declines in reproductive success, as breeding adults must spend more time and energy to find prey farther from the colony.1 Seabird colony size often varies over several orders of magnitude within the same species and can include millions of individuals per colony.5,6 As such, colony size likely plays an important role in determining the individual behavior of its members and how the colony interacts with the surrounding environment.6 Using tracking data from murres (Uria spp.), the world's most densely breeding seabirds, we show that the distribution of foraging-trip distances scales to colony size0.33 during the chick-rearing stage, consistent with Ashmole's halo theory.1,2 This pattern occurred across colonies varying in size over three orders of magnitude and distributed throughout the North Atlantic region. The strong relationship between colony size and foraging range means that the foraging areas of some colonial species can be estimated from colony sizes, which is more practical to measure over a large geographic scale. Two-thirds of the North Atlantic murre population breed at the 16 largest colonies; by extrapolating the predicted foraging ranges to sites without tracking data, we show that only two of these large colonies have significant coverage as marine protected areas. Our results are an important example of how theoretical models, in this case, Ashmole's version of central-place-foraging theory, can be applied to inform conservation and management in colonial breeding species.

Accelerating animal energetics: high dive costs in a small seabird disrupt the dynamic body acceleration-energy expenditure relationship.

Accelerometry has been widely used to estimate energy expenditure in a broad array of terrestrial and aquatic species. However, a recent reappraisal of the method showed that relationships between dynamic body acceleration (DBA) and energy expenditure weaken as the proportion of non-mechanical costs increases. Aquatic air breathing species often exemplify this pattern, as buoyancy, thermoregulation and other physiological mechanisms disproportionately affect oxygen consumption during dives. Combining biologging with the doubly labelled water method, we simultaneously recorded daily energy expenditure (DEE) and triaxial acceleration in one of the world's smallest wing-propelled breath-hold divers, the dovekie (Alle alle). These data were used to estimate the activity-specific costs of flying and diving and to test whether overall dynamic body acceleration (ODBA) is a reliable predictor of DEE in this abundant seabird. Average DEE for chick-rearing dovekies was 604±119 kJ day-1 across both sampling years. Despite recording lower stroke frequencies for diving than for flying (in line with allometric predictions for auks), dive costs were estimated to surpass flight costs in our sample of birds (flying: 7.24× basal metabolic rate, BMR; diving: 9.37× BMR). As expected, ODBA was not an effective predictor of DEE in this species. However, accelerometer-derived time budgets did accurately estimate DEE in dovekies. This work represents an empirical example of how the apparent energetic costs of buoyancy and thermoregulation limit the effectiveness of ODBA as the sole predictor of overall energy expenditure in small shallow-diving endotherms.

Mercury, legacy and emerging POPs, and endocrine-behavioural linkages: Implications of Arctic change in a diving seabird.

Arctic species encounter multiple stressors including climate change and environmental contaminants. Some contaminants may disrupt hormones that govern the behavioural responses of wildlife to climatic variation, and thus the capacity of species to respond to climate change. We investigated correlative interactions between legacy and emerging persistent organic pollutants (POPs), mercury (Hg), hormones and behaviours, in thick-billed murres (Uria lomvia) (N = 163) breeding in northern Hudson Bay (2016-2018). The blood profile of the murres was dominated by methylmercury (MeHg), followed by much lower levels of sum (∑) 35 polychlorinated biphenyls (PCBs), hexachlorobenzene (HCB) and p,p'-dichlorodiphenyltrichloroethylene (DDE), polybrominated diphenyl ethers (PBDEs) BDE-47, -99 and BDE-100; all other measured organochlorine pesticides and replacement brominated flame retardants had low concentrations if detected. Inter-annual variations occurred in MeHg, circulating triiodothyronine (T3), thyroxine (T4), and the foraging behaviours of the murres, identified using GPS-accelerometers. Compared to the 50-year mean date (1971-2021) for 50% of sea-ice coverage in Hudson Bay, sea-ice breakup was 1-2 weeks earlier (2016, 2017) or comparable (2018). Indeed, 2017 was the earliest year on record. Consistent with relationships identified individually between MeHg and total T3, and T3 and foraging behaviour, a direct interaction between these three parameters was evident when all possible interactions among measured chemical pollutants, hormones, and behaviours of the murres were considered collectively (path analysis). When murres were likely already stressed due to early sea-ice breakup (2016, 2017), blood MeHg influenced circulating T3 that in turn reduced foraging time underwater. We conclude that when sea-ice breaks up early in the breeding season, Hg may interfere with the ability of murres to adjust their foraging behaviour via T3 in relation to variation in sea-ice.

Potential disruption of thyroid hormones by perfluoroalkyl acids in an Arctic seabird during reproduction.

Arctic marine ecosystems are experiencing rapid change, such as ocean warming and enhanced pollutants. Perfluoroalkyl acids (PFAAs) arriving via long-range transport have been detected in Arctic wildlife, including seabirds which are considered sentinels of marine ecosystem health. There is evidence that PFAA exposure leads to the disruption of thyroid hormones (THs), such as thyroxine (T4) and triiodothyronine (T3), which play important roles in metabolism, incubation, and thermoregulation in seabirds. Here, we investigated relationships between PFAAs and THs [total T4 (TT4), free T4 (FT4), total T3 (TT3) and free T3 (FT3)] in blood plasma collected from 63 thick-billed murres (Uria lomvia) at a colony located in northern Hudson Bay (2016-2018). We then tested if PFAAs and TH levels were related to fitness-associated reproductive traits, such as body mass and hatch dates. PFUdA, PFOS, and PFTrDA were the dominant PFAAs in murre blood, accounting for approximately 77% of ∑PFAA. Females had higher PFAAs than males, possibly due to higher trophic feeding. While FT3 increased with PFOS, PFNA, PFDA, PFDoA, PFTeDA, ∑PFCA7, and ∑PFAA in murres, TT3 decreased with PFOS, PFDoA, and PFTeDA in males, but not females, suggesting thyroid disruption. TT3 increased with body mass, whereas several long-chain PFAAs were negatively correlated with body mass. Negative relationships between PFNA, PFDoA, PFTrDA, PFTeDA, and ∑PFAA with hatch dates may be the result of a disruption in incubation behaviour, resulting in earlier hatch dates. Consequently, TT3 concentrations were highest in males and females in 2018, a year in which PFAAs were lowest and hatch dates were delayed relative to 2017. As an Arctic seabird experiencing several indirect effects of climate change, the interaction of PFAAs on thyroid activity may cause additional stress to murres.

Altered Oxidative Status as a Cost of Reproduction in a Seabird with High Reproductive Costs.

AbstractLife history theory posits that reproduction is constrained by a cost of reproduction such that any increase in breeding effort should reduce subsequent survival. Oxidative stress refers to an imbalance between the prooxidant reactive oxygen species (ROS) and antioxidant defense. If not thwarted, ROS can cause damage to DNA, lipids, and proteins, potentially increasing the rate of senescence and decreasing cellular function. Reproduction is often associated with higher metabolic rates, which could increase production of ROS and lead to oxidative damage if the animal does not increase antioxidant protection. Thus, oxidative stress could be one mechanism creating a cost of reproduction. In this study we explored how reproduction may affect oxidative status differently between male and female thick-billed murres during early and late breeding seasons over three consecutive years. We manipulated breeding efforts by removing an egg from the nest of some individuals, which forced females to relay, and by handicapping other individuals by clipping wings. We measured total antioxidant capacity (TAC), uric acid (UA) concentration, and malondialdehyde (MDA; an index of lipid oxidative damage) concentration in blood plasma as well as activities of superoxide dismutase (SOD), glutathione peroxidase (GPx), and catalase (CAT) in red blood cells. Oxidative status was highly variable across years, and year was consistently the most important factor determining oxidative status; inconsistent results in previous field studies may be because reproductive oxidative stress occurs only in some years. Females had lower SOD and GPx and higher MDA and TAC than males immediately after egg laying, suggesting that the cost of egg laying required investment in cheaper nonenzymatic antioxidant defenses that had lower capacity for defending against lipid peroxidation. Delayed birds had lower UA and lower SOD, GPx, and CAT activity compared with control birds. In conclusion, when reproductive costs increase via higher energy costs or longer breeding seasons, the oxidative status of both male and female murres deteriorated as a result of reduced antioxidant defenses.

Seasonal variation of mercury contamination in Arctic seabirds: A pan-Arctic assessment.

Mercury (Hg) is a natural trace element found in high concentrations in top predators, including Arctic seabirds. Most current knowledge about Hg concentrations in Arctic seabirds relates to exposure during the summer breeding period when researchers can easily access seabirds at colonies. However, the few studies focused on winter have shown higher Hg concentrations during the non-breeding period than breeding period in several tissues. Hence, improving knowledge about Hg exposure during the non-breeding period is crucial to understanding the threats and risks encountered by these species year-round. We used feathers of nine migratory alcid species occurring at high latitudes to study bird Hg exposure during both the breeding and non-breeding periods. Overall, Hg concentrations during the non-breeding period were ~3 times higher than during the breeding period. In addition, spatial differences were apparent within and between the Atlantic and Pacific regions. While Hg concentrations during the non-breeding period were ~9 times and ~3 times higher than during the breeding period for the West and East Atlantic respectively, Hg concentrations in the Pacific during the non-breeding period were only ~1.7 times higher than during the breeding period. In addition, individual Hg concentrations during the non-breeding period for most of the seabird colonies were above 5 µg g-1 dry weight (dw), which is considered to be the threshold at which deleterious effects are observed, suggesting that some breeding populations might be vulnerable to non-breeding Hg exposure. Since wintering area locations, and migration routes may influence seasonal Hg concentrations, it is crucial to improve our knowledge about spatial ecotoxicology to fully understand the risks associated with Hg contamination in Arctic seabirds.

Accelerometry predicts muscle ultrastructure and flight capabilities in a wild bird.

Muscle ultrastructure is closely linked with athletic performance in humans and lab animals, and presumably plays an important role in the movement ecology of wild animals. Movement is critical for wild animals to forage, escape predators and reproduce. However, little evidence directly links muscle condition to locomotion in the wild. We used GPS-accelerometers to examine flight behaviour and muscle biopsies to assess muscle ultrastructure in breeding black-legged kittiwakes (Rissa tridactyla). Biopsied kittiwakes showed similar reproductive success and subsequent over-winter survival to non-biopsied kittiwakes, suggesting that our study method did not greatly impact foraging ability. Muscle fibre diameter was negatively associated with wing beat frequency, likely because larger muscle fibres facilitate powered flight. The number of nuclei per fibre was positively associated with average air speed, likely because higher power output needed by faster-flying birds required plasticity for muscle fibre recruitment. These results suggest the potential for flight behaviour to predict muscle ultrastructure.

A comparison of techniques for classifying behavior from accelerometers for two species of seabird.

The behavior of many wild animals remains a mystery, as it is difficult to quantify behavior of species that cannot be easily followed throughout their daily or seasonal movements. Accelerometers can solve some of these mysteries, as they collect activity data at a high temporal resolution (<1 s), can be relatively small (<1 g) so they minimally disrupt behavior, and are increasingly capable of recording data for long periods. Nonetheless, there is a need for increased validation of methods to classify animal behavior from accelerometers to promote widespread adoption of this technology in ecology. We assessed the accuracy of six different behavioral assignment methods for two species of seabird, thick-billed murres (Uria lomvia) and black-legged kittiwakes (Rissa tridactyla). We identified three behaviors using tri-axial accelerometers: standing, swimming, and flying, after classifying diving using a pressure sensor for murres. We evaluated six classification methods relative to independent classifications from concurrent GPS tracking data. We used four variables for classification: depth, wing beat frequency, pitch, and dynamic acceleration. Average accuracy for all methods was >98% for murres, and 89% and 93% for kittiwakes during incubation and chick rearing, respectively. Variable selection showed that classification accuracy did not improve with more than two (kittiwakes) or three (murres) variables. We conclude that simple methods of behavioral classification can be as accurate for classifying basic behaviors as more complex approaches, and that identifying suitable accelerometer metrics is more important than using a particular classification method when the objective is to develop a daily activity or energy budget. Highly accurate daily activity budgets can be generated from accelerometer data using multiple methods and a small number of accelerometer metrics; therefore, identifying a suitable behavioral classification method should not be a barrier to using accelerometers in studies of seabird behavior and ecology.