Indigo-dyed cellulose fibers and synthetic polymers in surface-feeding seabird chick regurgitates from the Gulf of Alaska.

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.

A Chromosome-Level Reference Genome for the Black-Legged Kittiwake (Rissa tridactyla), a Declining Circumpolar Seabird.

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 5× 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.

Optimization of dynamic soaring in a flap-gliding seabird affects its large-scale distribution at sea.

Dynamic soaring harvests energy from a spatiotemporal wind gradient, allowing albatrosses to glide over vast distances. However, its use is challenging to demonstrate empirically and has yet to be confirmed in other seabirds. Here, we investigate how flap-gliding Manx shearwaters optimize their flight for dynamic soaring. We do so by deriving a new metric, the horizontal wind effectiveness, that quantifies how effectively flight harvests energy from a shear layer. We evaluate this metric empirically for fine-scale trajectories reconstructed from bird-borne video data using a simplified flight dynamics model. We find that the birds' undulations are phased with their horizontal turning to optimize energy harvesting. We also assess the opportunity for energy harvesting in long-range, GPS-logged foraging trajectories and find that Manx shearwaters optimize their flight to increase the opportunity for dynamic soaring during favorable wind conditions. Our results show how small-scale dynamic soaring affects large-scale Manx shearwater distribution at sea.

Geolocators link marine mercury with levels in wild seabirds throughout their annual cycle: Consequences for trans-ecosystem biotransport.

Seabirds are widely used as indicators of marine pollution, including mercury (Hg), because they track contaminant levels across space and time. However, many seabirds are migratory, and it is difficult to understand the timing and location of their Hg accumulation. Seabirds may obtain Hg thousands of kilometers away, during their non-breeding period, and deposit that Hg into their terrestrial breeding colonies. We predicted that Hg concentration in rectrices reflects exposure during the previous breeding season, in body feathers reflects non-breeding exposure, and in blood collected during breeding reflects exposure during current breeding. To test this hypothesis, we measured total Hg concentration in these three tissues, which reflect different timepoints during the annual cycle of rhinoceros auklets (Cerorhinca monocerata) breeding on both sides of the North Pacific (Middleton Island in Alaska and Teuri Island in Hokkaido), and tracked their wintering movement patterns with biologging devices. We (i) identify the wintering patterns of both populations, (ii) examine Hg levels in different tissues representing exposure at different time periods, (iii) test how environmental Hg exposure during the non-breeding season affects bird contamination, and (iv) assess whether variation in Hg levels during the non-breeding season influences levels accumulated in terrestrial plants. Individuals from both populations followed a figure-eight looping migration pattern. We confirm the existence of a pathway from environmental Hg to plant roots via avian tissues, as Hg concentrations were higher in plants within the auklet colonies than at control sites. Hg concentrations of breast feathers were higher in Alaskan than in Japanese auklets, but Hg concentrations in rectrices and blood were similar. Moreover, we found evidence that tissues with different turnover rates could record local anthropogenic Hg emission rates of areas visited during winter. In conclusion, Hg was transported across thousands of kilometers by seabirds and transferred to local plants.

Short-term behavioural impact contrasts with long-term fitness consequences of biologging in a long-lived seabird.

Biologging has emerged as one of the most powerful and widely used technologies in ethology and ecology, providing unprecedented insight into animal behaviour. However, attaching loggers to animals may alter their behaviour, leading to the collection of data that fails to represent natural activity accurately. This is of particular concern in free-ranging animals, where tagged individuals can rarely be monitored directly. One of the most commonly reported measures of impact is breeding success, but this ignores potential short-term alterations to individual behaviour. When collecting ecological or behavioural data, such changes can have important consequences for the inference of results. Here, we take a multifaceted approach to investigate whether tagging leads to short-term behavioural changes, and whether these are later reflected in breeding performance, in a pelagic seabird. We analyse a long-term dataset of tracking data from Manx shearwaters (Puffinus puffinus), comparing the effects of carrying no device, small geolocator (GLS) devices (0.6% body mass), large Global Positioning System (GPS) devices (4.2% body mass) and a combination of the two (4.8% body mass). Despite exhibiting normal breeding success in both the year of tagging and the following year, incubating birds carrying GPS devices altered their foraging behaviour compared to untagged birds. During their foraging trips, GPS-tagged birds doubled their time away from the nest, experienced reduced foraging gains (64% reduction in mass gained per day) and reduced flight time by 14%. These findings demonstrate that the perceived impacts of device deployment depends on the scale over which they are sought: long-term measures, such as breeding success, can obscure finer-scale behavioural change, potentially limiting the validity of using GPS to infer at-sea behaviour when answering behavioural or ecological questions.

Shearwaters know the direction and distance home but fail to encode intervening obstacles after free-ranging foraging trips.

While displacement experiments have been powerful for determining the sensory basis of homing navigation in birds, they have left unresolved important cognitive aspects of navigation such as what birds know about their location relative to home and the anticipated route. Here, we analyze the free-ranging Global Positioning System (GPS) tracks of a large sample (n = 707) of Manx shearwater, Puffinus puffinus, foraging trips to investigate, from a cognitive perspective, what a wild, pelagic seabird knows as it begins to home naturally. By exploiting a kind of natural experimental contrast (journeys with or without intervening obstacles) we first show that, at the start of homing, sometimes hundreds of kilometers from the colony, shearwaters are well oriented in the homeward direction, but often fail to encode intervening barriers over which they will not fly (islands or peninsulas), constrained to flying farther as a result. Second, shearwaters time their homing journeys, leaving earlier in the day when they have farther to go, and this ability to judge distance home also apparently ignores intervening obstacles. Thus, at the start of homing, shearwaters appear to be making navigational decisions using both geographic direction and distance to the goal. Since we find no decrease in orientation accuracy with trip length, duration, or tortuosity, path integration mechanisms cannot account for these findings. Instead, our results imply that a navigational mechanism used to direct natural large-scale movements in wild pelagic seabirds has map-like properties and is probably based on large-scale gradients.

Flight costs in volant vertebrates: A phylogenetically-controlled meta-analysis of birds and bats.

Flight costs play an important role in determining the behavior, ecology, and physiology of birds and bats. Mechanical flight costs can be estimated from aerodynamics. However, measured metabolic flight costs (oxygen consumption rate) are less accurately predicted by flight theory, either because of (1) variation in flight efficiency across species, (2) variation in how basal costs interact with flight costs or (3) methodological biases. To tease apart these three hypotheses, we conducted a phylogenetically-controlled meta-analysis based on data from birds and bats. Birds doing short flights in a lab had higher metabolic rates than those with sustained flapping flight. In turn, species that used sustained flapping flight had a higher metabolic rate than those that flew primarily via gliding. Models accounting for relatedness (phylogeny) explained the data better than those that did not, which is congruent with the idea that several different flight Bauplans have evolved within birds and bats. Focusing on species with sustained flapping flight, for which more data are currently available, we found that flight cost estimates were not affected by measurement methods in both birds and bats. However, efficiency increased with body mass and decreased with flight speed in both birds and bats. Basal metabolic rate was additive to flight metabolic rate in bats but not birds. We use these results to derive an equation for estimating metabolic flight costs of birds and bats that includes variation in whole animal efficiency with flight speed and body mass.

Global Monitoring of Persistent Organic Pollutants (POPs) Using Seabird Preen Gland Oil.

Situated at high positions on marine food webs, seabirds accumulate high concentrations of persistent organic pollutants (POPs), such as polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane and its metabolites (DDTs), and hexachlorocyclohexanes (HCHs). Our previous studies proposed the usefulness of seabirds preen gland oil as a nondestructive biomonitoring tool. The present study applied this approach to 154 adult birds of 24 species collected from 11 locations during 2005-2016 to demonstrate the utility of preen gland oil as a tool for global monitoring POPs, i.e., PCBs, DDTs, and HCHs. Concentrations of the POPs were higher in the Northern Hemisphere than in the Southern Hemisphere. In particular, ∑20PCBs and∑DDTs were highly concentrated in European shags (Phalacrocorax aristotelis) and Japanese cormorants (Phalacrocorax capillatus), explainable by a diet of benthic fishes. Higher concentrations of γ-HCH were detected in species from the polar regions, possibly reflecting the recent exposure and global distillation of ∑HCHs. We examined the relationship between age and POP concentrations in preen gland oil from 20 male European shags, aged 3-16 years old. Concentrations and compositions of POPs were not related to age. We also examined sex differences in the POP concentrations from 24 streaked shearwaters (Calonectris leucomelas) and did not detect a sex bias. These results underline the importance of the geographic concentration patterns and the dietary behavior as determinants species-specific POPs concentrations in preen gland oil.

Concomitant Regulation by a LacI-Type Transcriptional Repressor XylR on Genes Involved in Xylan and Xylose Metabolism and the Type III Secretion System in Rice Pathogen Xanthomonas oryzae pv. oryzae.

The hypersensitive response and pathogenicity (hrp) genes of Xanthomonas oryzae pv. oryzae, the causal agent of bacterial leaf blight of rice, encode components of the type III secretion system and are essential for virulence. Expression of hrp genes is regulated by two key hrp regulators, HrpG and HrpX; HrpG regulates hrpX and hrpA, and HrpX regulates the other hrp genes on hrpB-hrpF operons. We previously reported the sugar-dependent quantitative regulation of HrpX; the regulator highly accumulates in the presence of xylose, followed by high hrp gene expression. Here, we found that, in a mutant lacking the LacI-type transcriptional regulator XylR, HrpX accumulation and hrp gene expression were high even in the medium without xylose, reaching the similar levels present in the wild type incubated in the xylose-containing medium. XylR also negatively regulated one of two xylose isomerase genes (xylA2 but not xylA1) by binding to the motif sequence in the upstream region of the gene. Xylose isomerase is an essential enzyme in xylose metabolism and interconverts between xylose and xylulose. Our results suggest that, in the presence of xylose, inactivation of XylR leads to greater xylan and xylose utilization and, simultaneously, to higher accumulation of HrpX, followed by higher hrp gene expression in the bacterium.

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.

Remotely sensed wind speed predicts soaring behaviour in a wide-ranging pelagic seabird.

Global wind patterns affect flight strategies in many birds, including pelagic seabirds, many of which use wind-powered soaring to reduce energy costs during at-sea foraging trips and migration. Such long-distance movement patterns are underpinned by local interactions between wind conditions and flight behaviour, but these fine-scale relationships are far less well understood. Here we show that remotely sensed ocean wind speed and direction are highly significant predictors of soaring behaviour in a migratory pelagic seabird, the Manx shearwater (Puffinus puffinus). We used high-frequency GPS tracking data (10 Hz) and statistical behaviour state classification to identify two energetic modes in at-sea flight, corresponding to flap-like and soar-like flight. We show that soaring is significantly more likely to occur in tailwinds and crosswinds above a wind speed threshold of around 8 m s-1, suggesting that these conditions enable birds to reduce metabolic costs by preferentially soaring over flapping. Our results suggest a behavioural mechanism by which wind conditions may shape foraging and migration ecology in pelagic seabirds, and thus indicate that shifts in wind patterns driven by climate change could impact this and other species. They also emphasize the emerging potential of high-frequency GPS biologgers to provide detailed quantitative insights into fine-scale flight behaviour in free-living animals.

Breeding density, fine-scale tracking, and large-scale modeling reveal the regional distribution of four seabird species.

Population-level estimates of species' distributions can reveal fundamental ecological processes and facilitate conservation. However, these may be difficult to obtain for mobile species, especially colonial central-place foragers (CCPFs; e.g., bats, corvids, social insects), because it is often impractical to determine the provenance of individuals observed beyond breeding sites. Moreover, some CCPFs, especially in the marine realm (e.g., pinnipeds, turtles, and seabirds) are difficult to observe because they range tens to ten thousands of kilometers from their colonies. It is hypothesized that the distribution of CCPFs depends largely on habitat availability and intraspecific competition. Modeling these effects may therefore allow distributions to be estimated from samples of individual spatial usage. Such data can be obtained for an increasing number of species using tracking technology. However, techniques for estimating population-level distributions using the telemetry data are poorly developed. This is of concern because many marine CCPFs, such as seabirds, are threatened by anthropogenic activities. Here, we aim to estimate the distribution at sea of four seabird species, foraging from approximately 5,500 breeding sites in Britain and Ireland. To do so, we GPS-tracked a sample of 230 European Shags Phalacrocorax aristotelis, 464 Black-legged Kittiwakes Rissa tridactyla, 178 Common Murres Uria aalge, and 281 Razorbills Alca torda from 13, 20, 12, and 14 colonies, respectively. Using Poisson point process habitat use models, we show that distribution at sea is dependent on (1) density-dependent competition among sympatric conspecifics (all species) and parapatric conspecifics (Kittiwakes and Murres); (2) habitat accessibility and coastal geometry, such that birds travel further from colonies with limited access to the sea; and (3) regional habitat availability. Using these models, we predict space use by birds from unobserved colonies and thereby map the distribution at sea of each species at both the colony and regional level. Space use by all four species' British breeding populations is concentrated in the coastal waters of Scotland, highlighting the need for robust conservation measures in this area. The techniques we present are applicable to any CCPF.

Carry-over effects on the annual cycle of a migratory seabird: an experimental study.

Long-lived migratory animals must balance the cost of current reproduction with their own condition ahead of a challenging migration and future reproduction. In these species, carry-over effects, which occur when events in one season affect the outcome of the subsequent season, may be particularly exacerbated. However, how carry-over effects influence future breeding outcomes and whether (and how) they also affect behaviour during migration and wintering is unclear. Here we investigate carry-over effects induced by a controlled, bidirectional manipulation of the duration of reproductive effort on the migratory, wintering and subsequent breeding behaviour of a long-lived migratory seabird, the Manx shearwater Puffinus puffinus. By cross-fostering chicks of different age between nests, we successfully prolonged or shortened by ∼25% the chick-rearing period of 42 breeding pairs. We tracked the adults with geolocators over the subsequent year and combined migration route data with at-sea activity budgets obtained from high-resolution saltwater-immersion data. Migratory behaviour was also recorded during non-experimental years (the year before and/or two years after manipulation) for a subset of birds, allowing comparison between experimental and non-experimental years within treatment groups. All birds cared for chicks until normal fledging age, resulting in birds with a longer breeding period delaying their departure on migration; however, birds that finished breeding earlier did not start migrating earlier. Increased reproductive effort resulted in less time spent at the wintering grounds, a reduction in time spent resting daily and a delayed start of breeding with lighter eggs and chicks and lower breeding success the following breeding season. Conversely, reduced reproductive effort resulted in more time resting and less time foraging during the winter, but a similar breeding phenology and success compared with control birds the following year, suggesting that 'positive' carry-over effects may also occur but perhaps have a less long-lasting impact than those incurred from increased reproductive effort. Our results shed light on how carry-over effects can develop and modify an adult animal's behaviour year-round and reveal how a complex interaction between current and future reproductive fitness, individual condition and external constraints can influence life-history decisions.

Drivers and fitness consequences of dispersive migration in a pelagic seabird.

Animals can be flexible in their migration strategies, using several wintering sites or a variety of routes. The mechanisms promoting the development of these migratory patterns and their potential fitness consequences are poorly understood. Here, we address these questions by tracking the dispersive migration of a pelagic seabird, the Atlantic puffin Fratercula arctica, using over 100 complete migration tracks collected over 7 years, including repeated tracks of individuals for up to 6 consecutive years. Because puffins have high flight costs, dispersion may generate important variation in costs of migration. We investigate differences in activity budgets and energy expenditure between different strategies. We find that puffins visit a range of overwintering destinations, resulting in a diversity of migratory routes differing in energy expenditures; however, they show interindividual similarity in the timings and location of major movements. We consider 3 hypothetical mechanisms that could generate this pattern: 1) random dispersion; 2) sex segregation; and 3) intraspecific competition or differences in individual quality. First, we dismiss random dispersion because individuals show strong route fidelity between years. Second, we find that sex differences contribute to, but do not account fully for, the migratory variation observed. Third, we find significant differences in breeding success between overwintering destinations, which, together with differences in foraging levels between routes, suggest that birds of different quality may visit different destinations. Taken together, our results show that dispersive migration is a complex phenomenon that can be driven by multiple factors simultaneously and can shape a population's fitness landscape.

Foraging flexibility and search patterns are unlinked during breeding in a free-ranging seabird.

In order to maximize foraging efficiency in a varying environment, predators are expected to optimize their search strategy. Environmental conditions are one important factor affecting these movement patterns, but variations in breeding constraints (self-feeding vs. feeding young and self-feeding) during different breeding stages (incubation vs. chick-rearing) are often overlooked, so that the mechanisms responsible for such behavioral shifts are still unknown. Here, to test how search patterns are affected at different breeding stages and to explore the proximate causes of these variations, we deployed data loggers to record both position (global positioning system) and dive activity (time-depth recorders) of a colonial breeding seabird, the razorbill Alca torda. Over a period of 3 years, our recordings of 56 foraging trips from 18 breeders show that while there is no evidence for individual route fidelity, razorbills exhibit higher foraging flexibility during incubation than during chick rearing, when foraging becomes more focused on an area of high primary productivity. We further show that this behavioral shift is not due to a shift in search patterns, as reorientations during foraging are independent of breeding stage. Our results suggest that foraging flexibility and search patterns are unlinked, perhaps because birds can read cues from their environment, including conspecifics, to optimize their foraging efficiency.

Dual foraging and pair coordination during chick provisioning by Manx shearwaters: empirical evidence supported by a simple model.

The optimal allocation of time and energy between one's own survival and offspring survival is critical for iteroparous animals, but creates a conflict between what maximises the parent's fitness and what maximises fitness of the offspring. For central-place foragers, provisioning strategies may reflect this allocation, while the distance between central-places and foraging areas may influence the decision. Nevertheless, few studies have explored the link between life history and foraging in the context of resource allocation. Studying foraging behaviour alongside food load rates to chicks provides a useful system for understanding the foraging decisions made during parent-offspring conflict. Using simultaneously deployed GPS and time-depth recorders, we examined the provisioning strategies in free-living Manx shearwaters Puffinus puffinus, which were caring for young. Our results showed a bimodal pattern, where birds alternate short and long trips. Short trips were associated with higher feeding frequency and larger meals than long trips, suggesting that long trips were performed for self-feeding. Furthermore, most foraging was carried out within 100 km of sea fronts. A simple model based on patch quality and travel time shows that for Manx shearwaters combining chick feeding and self-maintenance, bimodal foraging trip durations optimise feeding rates.

High corticosterone, not high energy cost, correlates with reproductive success in the burrow-nesting ancient murrelet.

Theory and observations suggest that offspring abandonment in animals may occur when the costs to future reproductive output of current reproductive effort outweigh the fitness benefits of rearing the current brood. While hormonal cues (i.e. corticosterone) or energy reserves are believed to be involved, few studies have directly focused on the proximate cues influencing behaviours directly related to reproductive success. To address this information gap, we determined the incubation metabolic rates and corticosterone (CORT) levels of naturally fasting and freely incubating ancient murrelets (Synthliboramphus antiquus). Respiratory quotient (RQ) increased with date, suggesting that incubating ancient murrelets shifted from strictly lipid-based metabolism towards more protein-based metabolism as incubation progressed. Birds that hatched only one nestling had higher levels of circulating CORT than those which hatched two, suggesting that birds which laid only a single egg found incubation more stressful than those which laid two. However, CORT levels and incubation shift lengths were not correlated, suggesting that birds that undertook prolonged incubation shifts did so only when their energy stores were not jeopardized.

Incubation patterns in a central-place forager affect lifetime reproductive success: scaling of patterns from a foraging bout to a lifetime.

BACKGROUND: Long-lived seabirds face a conflict between current and lifelong reproductive success. During incubation shifts, egg neglect is sometimes necessary to avoid starvation, but may compromise the current reproductive attempt. However, factors underlying this decision process are poorly understood. We focus on the ancient murrelet, Synthliboramphus antiquus, an alcid with exceptionally long incubation shift lengths, and test the impact of environmental factors on incubation shift length in relation to reproductive success. METHODOLOGY/PRINCIPAL FINDINGS: Using an information theoretic approach, we show that incubation shift length was a strong predictor of reproductive success for ancient murrelets at Reef Island, Haida Gwaii, British Columbia, Canada during the 2007 and 2008 breeding seasons. The most important factors explaining an individual's shift length were egg size, wind speed and the length of the mate's previous shift. Wind speed and tide height were the two most important factors for determining foraging behavior, as measured by dive frequency and depth. CONCLUSIONS/SIGNIFICANCE: Our study demonstrates that (i) species-specific reproductive strategies interact with environmental conditions such as wind speed to form multiple incubation patterns and (ii) maintaining regular incubation shifts is an essential component of reproductive success.