Biochemical and molecular biomarkers and their association with anthropogenic chemicals in wintering Manx shearwaters (Puffinus puffinus).

Anthropogenic pollution poses a threat to marine conservation by causing chronic toxic effects. Seabirds have contact throughout their lives with pollutants like plastic, metals, polychlorinated biphenyls (PCBs), and organochlorine pesticides such as hexachlorocyclohexanes (HCHs). We assessed 155 Manx shearwaters (Puffinus puffinus) stranded along the Brazilian coast, analyzing associations between organic pollutants, plastic ingestion, biomarkers (transcript levels of aryl hydrocarbon receptor, cytochrome P450-1A-5 [CYP1A5], UDP-glucuronosyl-transferase [UGT1], estrogen receptor alpha-1 [ESR1], and heat shock protein-70 genes) and enzymes activity (ethoxy-resorufin O-deethylase and glutathione S-transferase [GST]). Plastic debris was found in 29 % of the birds. The transcription of UGT1 and CYP1A5 was significantly associated with hexachlorobenzene (HCB) and PCBs levels. ESR1 was associated with HCB and Mirex, and GST was associated with Drins and Mirex. While organic pollutants affected shearwaters more than plastic ingestion, reducing plastic availability remains relevant as xenobiotics are also potentially adsorbed onto plastics.

Climate change drives migratory range shift via individual plasticity in shearwaters.

How individual animals respond to climate change is key to whether populations will persist or go extinct. Yet, few studies investigate how changes in individual behavior underpin these population-level phenomena. Shifts in the distributions of migratory animals can occur through adaptation in migratory behaviors, but there is little understanding of how selection and plasticity contribute to population range shift. Here, we use long-term geolocator tracking of Balearic shearwaters (Puffinus mauretanicus) to investigate how year-to-year changes in individual birds' migrations underpin a range shift in the post-breeding migration. We demonstrate a northward shift in the post-breeding range and show that this is brought about by individual plasticity in migratory destination, with individuals migrating further north in response to changes in sea-surface temperature. Furthermore, we find that when individuals migrate further, they return faster, perhaps minimizing delays in return to the breeding area. Birds apparently judge the increased distance that they will need to migrate via memory of the migration route, suggesting that spatial cognitive mechanisms may contribute to this plasticity and the resulting range shift. Our study exemplifies the role that individual behavior plays in populations' responses to environmental change and highlights some of the behavioral mechanisms that might be key to understanding and predicting species persistence in response to climate change.

How do resource distribution and taxonomy affect the use of dual foraging in seabirds? A review.

In many seabird species, parents feeding young switch between short and long foraging excursions in a strategy known as "dual foraging." To investigate whether habitat quality near breeding colonies drives the use of dual foraging, we conducted a review of the seabird literature, compiling the results of 102 studies which identified dual-foraging in 50 species across nine families from all six seabird orders. We estimated the mean distance from the colony of each species' short and long foraging trips and obtained remote-sensed data on chlorophyll-a concentrations within the radius of both short and long trips around each colony. We then assessed, for each seabird family, the relationship between the use of dual foraging strategies and the difference in the quality of foraging locations between short- and long-distance foraging trips. We found that the probability of dual foraging grew with increasing differences in the quality of foraging locations available during short- and long-distance trips. We also found that when controlling for differences in habitat quality, albatrosses and penguins were less likely to use dual foraging than Procellariidae, which in turn were less likely to use dual foraging than Sulids. This study helps clarify how environmental conditions and taxon-specific characteristics influence seabird foraging behavior.

A new biologging approach reveals unique flightless molt strategies of Atlantic puffins.

Animal-borne telemetry devices provide essential insights into the life-history strategies of far-ranging species and allow us to understand how they interact with their environment. Many species in the seabird family Alcidae undergo a synchronous molt of all primary flight feathers during the non-breeding season, making them flightless and more susceptible to environmental stressors, including severe storms and prey shortages. However, the timing and location of molt remain largely unknown, with most information coming from studies on birds killed by storms or shot by hunters for food. Using light-level geolocators with saltwater immersion loggers, we develop a method for determining flightless periods in the context of the annual cycle. Four Atlantic puffins (Fratercula arctica) were equipped with geolocator/immersion loggers on each leg to attempt to overcome issues of leg tucking in plumage while sitting on the water, which confounds the interpretation of logger data. Light-level and saltwater immersion time-series data were combined to correct for this issue. This approach was adapted and applied to 40 puffins equipped with the standard practice deployments of geolocators on one leg only. Flightless periods consistent with molt were identified in the dual-equipped birds, whereas molt identification in single-equipped birds was less effective and definitive and should be treated with caution. Within the dual-equipped sample, we present evidence for two flightless molt periods per non-breeding season in two puffins that undertook more extensive migrations (>2000 km) and were flightless for up to 77 days in a single non-breeding season. A biannual flight feather molt is highly unusual among non-passerine birds and may be unique to birds that undergo catastrophic molt, i.e., become flightless when molting. Although our conclusions are based on a small sample, we have established a freely available methodological framework for future investigation of the molt patterns of this and other seabird species.

Case Report of Puffinosis in a Manx Shearwater (Puffinus puffinus) Suggesting Environmental Aetiology.

Puffinosis is a disease of a range of seabirds characterised by dorsal and ventral blistering of their webbed feet, conjunctivitis, dry necrosis, leg spasticity, head shaking, loss of balance, tremors, and death. It is associated with Manx shearwaters (Puffinus puffinus), frequently affecting chicks within their underground nesting burrows. The aetiology of the disease is unclear but has been attributed to a type-2 coronavirus associated with Neotombicula mites as a potential vector. However, there is some uncertainty given potential laboratory contamination with mouse hepatitis virus and failure to fulfil Koch's postulates, with birds injected with isolates remaining healthy. We describe a detailed case report of puffinosis in a Manx Shearwater covering necropsy, histology, bacteriology, and metagenomics including viral sequencing. We found no evidence of viral infection or parasites. Our results are consistent with an entirely environmental aetiology, with caustic faecal ammonia in damp nesting burrows causing conjunctivitis and foot dermatitis breaking the skin, allowing common soil bacteria (i.e., Flavobacterium, Staphylococcus and Serratia spp., Clostridia perfringens and Enterococcus faecalis) to cause opportunistic infection, debilitating the bird and leading to death. A similar condition (foot pad dermatitis or FPD) has been reported in broiler chickens, attributed to caustic faeces, high humidity, and poor environmental conditions during indoor rearing, preventable by adequate ventilation and husbandry. This is consistent with puffinosis being observed in Shearwater nesting burrows situated in tall, dense, vegetation (e.g., bracken Pteridium aquilinum) but rarely reported in burrows situated in well-ventilated, short coastal grasslands. This proposed environmental aetiology accounts for the disease's non-epizootic prevalence, spatial variation within colonies, and higher frequency in chicks that are restricted to nesting burrows.

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.

How might magnetic secular variation impact avian philopatry?

A tendency to return to the natal/breeding site, 'philopatry', is widespread amongst migratory birds. It has been suggested that a magnetic 'map' could underpin such movements, though it is unclear how a magnetic map might be impacted by gradual drift in the Earth's magnetic field ('secular variation'). Here, using the International Geomagnetic Reference Field, we quantified how secular variation translates to movement in the implied positions at which combinations of different magnetic cues (inclination, declination and intensity) intersect, noting that the magnitude of such movements is determined by the magnitude of the movements of each of the two isolines, and the angle between their movement vectors. We propose that magnetic parameters varying in a near-parallel arrangement are unlikely to be used as a bi-coordinate map during philopatry, but that birds could use near-orthogonal magnetic gradient cues as a bi-coordinate map if augmented with navigation using more local cues. We further suggest that uni-coordinate magnetic information could also provide a philopatry mechanism that is substantially less impacted by secular variation than a bi-coordinate 'map'. We propose that between-year shifts in the position of magnetic coordinates might provide a priori predictions for changes in the breeding sites of migratory birds.

Shearwaters sometimes take long homing detours when denied natural outward journey information.

The cognitive processes (learning and processing of information) underpinning the long-distance navigation of birds are poorly understood. Here, we used the homing motivation of the Manx shearwater to investigate navigational decision making in a wild bird by displacing them 294 km to the far side of a large island (the island of Ireland). Since shearwaters are reluctant to fly over land, the island blocked the direct route home, forcing a navigational decision. Further still, on the far side of the obstacle, we chose a release site where the use of local knowledge could facilitate a 20% improvement in route efficiency if shearwaters were able to anticipate and avoid a large inlet giving the appearance of open water in the home direction. We found that no shearwater took the most efficient initial route home, but instead oriented in the home direction (even once the obstacle became visible). Upon reaching the obstacle, four shearwaters subsequently circumnavigated the land mass via the long route, travelling a further 900 km as a result. Hence, despite readily orienting homewards immediately after displacement, shearwaters seem unaware of the scale of the obstacle formed by a large land mass despite this being a prominent feature of their regular foraging environment.

Unexpectedly deep diving in an albatross.

Albatrosses are the iconic aerial wanderers of the oceans, supremely adapted for long-distance dynamic soaring flight. Perhaps because of this they are considered poorly adapted for diving1, in contrast to many smaller shearwater and petrel relatives, despite having amphibious eyes2, and an a priori mass advantage for oxygen-storage tolerance3. Modern biologging studies have largely confirmed this view4,5, casting doubt on earlier observations using capillary tube maximum depth gauges1, which may exaggerate depths, and emphasising albatrosses' reliance on near-surface feeding. Nevertheless, uncertainty about albatross diving remains an important knowledge gap since bycatch in human fisheries (e.g. birds becoming hooked when diving for longline bait fish) is thought to be driving many population declines in this most threatened group of birds6. Here we show, using miniature electronic depth loggers (TDRs), that black-browed albatross, Thalassarche melanophris, can dive to much greater depths (19 m) and for much longer (52 s) than previously thought - three times the maxima previously recorded for this species (6 m and 15 s), and more than twice the maxima reliably recorded previously for any albatross (from 113.7 bird-days of tracking4,5,7). Further evidence that diving may be a significant behavioural adaptation in some albatrosses comes from co-deployed 3-axis accelerometers showing that these deeper dives, which occur in most individuals we tracked, involve active under-water propulsion without detectable initial assistance from momentum, sometimes with bottom phases typical of active prey pursuit. Furthermore, we find (from co-deployed GPS) that diving occurs primarily in the distal portions of long-distance foraging trips, with deeper dives occurring exclusively during daylight or civil twilight, confirming the importance of visual guidance.

Magnetic stop signs signal a European songbird's arrival at the breeding site after migration.

Although it is known that birds can return to their breeding grounds with exceptional precision, it has remained a mystery how they know when and where to stop migrating. Using nearly a century's worth of Eurasian reed warbler (Acrocephalus scirpaceus) ringing recoveries, we investigated whether fluctuations in Earth's magnetic field predict variation in the sites to which birds return. Ringing recoveries suggest that magnetic inclination is learned before departure and is subsequently used as a uni-coordinate "stop sign" when relocating the natal or breeding site. However, many locations have the same inclination angle. Data from populations with different migratory directions indicate that birds solve this ambiguity by stopping at the first place where the right inclination is encountered on an inherited return vector.

Demographic profiles and environmental drivers of variation relate to individual breeding state in a long-lived trans-oceanic migratory seabird, the Manx shearwater.

Understanding the points in a species breeding cycle when they are most vulnerable to environmental fluctuations is key to understanding interannual demography and guiding effective conservation and management. Seabirds represent one of the most threatened groups of birds in the world, and climate change and severe weather is a prominent and increasing threat to this group. We used a multi-state capture-recapture model to examine how the demographic rates of a long-lived trans-oceanic migrant seabird, the Manx shearwater Puffinus puffinus, are influenced by environmental conditions experienced at different stages of the annual breeding cycle and whether these relationships vary with an individual's breeding state in the previous year (i.e., successful breeder, failed breeder and non-breeder). Our results imply that populations of Manx shearwaters are comprised of individuals with different demographic profiles, whereby more successful reproduction is associated with higher rates of survival and breeding propensity. However, we found that all birds experienced the same negative relationship between rates of survival and wind force during the breeding season, indicating a cost of reproduction (or central place constraint for non-breeders) during years with severe weather conditions. We also found that environmental effects differentially influence the breeding propensity of individuals in different breeding states. This suggests individual spatio-temporal variation in habitat use during the annual cycle, such that climate change could alter the frequency that individuals with different demographic profiles breed thereby driving a complex and less predictable population response. More broadly, our study highlights the importance of considering individual-level factors when examining population demography and predicting how species may respond to climate change.

A magnet attached to the forehead disrupts magnetic compass orientation in a migratory songbird.

For studies on magnetic compass orientation and navigation performance in small bird species, controlled experiments with orientation cages inside an electromagnetic coil system are the most prominent methodological paradigm. These are, however, not applicable when studying larger bird species and/or orientation behaviour during free flight. For this, researchers have followed a very different approach, attaching small magnets to birds, with the intention of depriving them of access to meaningful magnetic information. Unfortunately, results from studies using this approach appear rather inconsistent. As these are based on experiments with birds under free-flight conditions, which usually do not allow exclusion of other potential orientation cues, an assessment of the overall efficacy of this approach is difficult to conduct. Here, we directly tested the efficacy of small magnets for temporarily disrupting magnetic compass orientation in small migratory songbirds using orientation cages under controlled experimental conditions. We found that birds which have access to the Earth's magnetic field as their sole orientation cue show a general orientation towards their seasonally appropriate migratory direction. When carrying magnets on their forehead under these conditions, the same birds become disoriented. However, under changed conditions that allow birds access to other (i.e. celestial) orientation cues, any disruptive effect of the magnets they carry appears obscured. Our results provide clear evidence for the efficacy of the magnet approach for temporarily disrupting magnetic compass orientation in birds, but also reveal its limitations for application in experiments under free-flight conditions.

Avoidance of different durations, colours and intensities of artificial light by adult seabirds.

There is increasing evidence for impacts of light pollution on the physiology and behaviour of wild animals. Nocturnally active Procellariiform seabirds are often found grounded in areas polluted by light and struggle to take to the air again without human intervention. Hence, understanding their responses to different wavelengths and intensities of light is urgently needed to inform mitigation measures. Here, we demonstrate how different light characteristics can affect the nocturnal flight of Manx shearwaters Puffinus puffinus by experimentally introducing lights at a colony subject to low levels of light pollution due to passing ships and coastal developments. The density of birds in flight above the colony was measured using a thermal imaging camera. We compared number of flying shearwaters under dark conditions and in response to an artificially introduced light, and observed fewer birds in flight during 'light-on' periods, suggesting that adult shearwaters were repelled by the light. This effect was stronger with higher light intensity, increasing duration of 'light-on' periods and with green and blue compared to red light. Thus, we recommend lower light intensity, red colour, and shorter duration of 'light-on' periods as mitigation measures to reduce the effects of light at breeding colonies and in their vicinity.

North Atlantic winter cyclones starve seabirds.

Each winter, the North Atlantic Ocean is the stage for numerous cyclones, the most severe ones leading to seabird mass-mortality events called "winter wrecks."1-3 During these, thousands of emaciated seabird carcasses are washed ashore along European and North American coasts. Winter cyclones can therefore shape seabird population dynamics4,5 by affecting survival rates as well as the body condition of surviving individuals and thus their future reproduction. However, most often the geographic origins of impacted seabirds and the causes of their deaths remain unclear.6 We performed the first ocean-basin scale assessment of cyclone exposure in a seabird community by coupling winter tracking data for ∼1,500 individuals of five key North Atlantic seabird species (Alle alle, Fratercula arctica, Uria aalge, Uria lomvia, and Rissa tridactyla) and cyclone locations. We then explored the energetic consequences of different cyclonic conditions using a mechanistic bioenergetics model7 and tested the hypothesis that cyclones dramatically increase seabird energy requirements. We demonstrated that cyclones of high intensity impacted birds from all studied species and breeding colonies during winter but especially those aggregating in the Labrador Sea, the Davis Strait, the surroundings of Iceland, and the Barents Sea. Our broad-scale analyses suggested that cyclonic conditions do not increase seabird energy requirements, implying that they die because of the unavailability of their prey and/or their inability to feed during cyclones. Our study provides essential information on seabird cyclone exposure in a context of marked cyclone regime changes due to global warming.8.

Foraging conditions for breeding penguins improve with distance from colony and progression of the breeding season at the South Orkney Islands.

BACKGROUND: According to central place foraging theory, animals will only increase the distance of their foraging trips if more distant prey patches offer better foraging opportunities. Thus, theory predicts that breeding seabirds in large colonies could create a zone of food depletion around the colony, known as "Ashmole's halo". However, seabirds' decisions to forage at a particular distance are likely also complicated by their breeding stage. After chicks hatch, parents must return frequently to feed their offspring, so may be less likely to visit distant foraging patches, even if their quality is higher. However, the interaction between prey availability, intra-specific competition, and breeding stage on the foraging decisions of seabirds is not well understood. The aim of this study was to address this question in chinstrap penguins Pygoscelis antarcticus breeding at a large colony. In particular, we aimed to investigate how breeding stage affects foraging strategy; whether birds foraging far from the colony visit higher quality patches than available locally; and whether there is evidence for intraspecific competition, indicated by prey depletions near the colony increasing over time, and longer foraging trips. METHODS: We used GPS and temperature-depth recorders to track the foraging movements of 221 chinstrap penguins from 4 sites at the South Orkney Islands during incubation and brood. We identified foraging dives and calculated the index of patch quality based on time allocation during the dive to assess the quality of the foraging patch. RESULTS: We found that chinstrap penguin foraging distance varied between stages, and that trips became shorter as incubation progressed. Although patch quality was lower near the colony than at more distant foraging patches, patch quality near the colony improved over the breeding season. CONCLUSIONS: These results suggest chinstrap penguin foraging strategies are influenced by both breeding stage and prey distribution, and the low patch quality near the colony may be due to a combination of depletion by intraspecific competition but compensated by natural variation in prey. Reduced trip durations towards the end of the incubation period may be due to an increase in food availability, as seabirds time their reproduction so that the period of maximum energy demand in late chick-rearing coincides with maximum resource availability in the environment. This may also explain why patch quality around the colony improved over the breeding season. Overall, our study sheds light on drivers of foraging decisions in colonial seabirds, an important question in foraging ecology.

Consistent concentrations of critically endangered Balearic shearwaters in UK waters revealed by at-sea surveys.

AIM: Europe's only globally critically endangered seabird, the Balearic shearwater (Puffinus mauretanicus), is thought to have expanded its postbreeding range northwards into UK waters, though its at sea distribution there is not yet well understood. This study aims to identify environmental factors associated with the species' presence, map the probability of presence of the species across the western English Channel and southern Celtic Sea, and estimate the number of individuals in this area. LOCATION: The western English Channel and southern Celtic Sea. METHODS: This study analyses strip transect data collected between 2013 and 2017 from vessel-based surveys in the western English Channel and southern Celtic Sea during the Balearic shearwater's postbreeding period. Using environmental data collected directly and from remote sensors both Generalized Additive Models and the Random Forest machine learning model were used to determine shearwater presence at different locations. Abundance was estimated separately using a density multiplication approach. RESULTS: Both models indicated that oceanographic features were better predictors of shearwater presence than fish abundance. Seafloor aspect, sea surface temperature, depth, salinity, and maximum current speed were the most important predictors. The estimated number of Balearic shearwaters in the prediction area ranged from 652 birds in 2017 to 6,904 birds in 2014. MAIN CONCLUSIONS: Areas with consistently high probabilities of shearwater presence were identified at the Celtic Sea front. Our estimates suggest that the study area in southwest Britain supports between 2% and 23% of the global population of Balearic shearwaters. Based on the timing of the surveys (mainly in October), it is probable that most of the sighted shearwaters were immatures. This study provides the most complete understanding of Balearic shearwater distribution in UK waters available to date, information that will help inform any future conservation actions concerning this endangered species.

Meeting Paris agreement objectives will temper seabird winter distribution shifts in the North Atlantic Ocean.

We explored the implications of reaching the Paris Agreement Objective of limiting global warming to <2°C for the future winter distribution of the North Atlantic seabird community. We predicted and quantified current and future winter habitats of five North Atlantic Ocean seabird species (Alle alle, Fratercula arctica, Uria aalge, Uria lomvia and Rissa tridactyla) using tracking data for ~1500 individuals through resource selection functions based on mechanistic modeling of seabird energy requirements, and a dynamic bioclimate envelope model of seabird prey. Future winter distributions were predicted to shift with climate change, especially when global warming exceed 2°C under a "no mitigation" scenario, modifying seabird wintering hotspots in the North Atlantic Ocean. Our findings suggest that meeting Paris agreement objectives will limit changes in seabird selected habitat location and size in the North Atlantic Ocean during the 21st century. We thereby provide key information for the design of adaptive marine-protected areas in a changing ocean.

Young frigatebirds learn how to compensate for wind drift.

Compensating for wind drift can improve goalward flight efficiency in animal taxa, especially among those that rely on thermal soaring to travel large distances. Little is known, however, about how animals acquire this ability. The great frigatebird (Fregata minor) exemplifies the challenges of wind drift compensation because it lives a highly pelagic lifestyle, travelling very long distances over the open ocean but without the ability to land on water. Using GPS tracks from fledgling frigatebirds, we followed young frigatebirds from the moment of fledging to investigate whether wind drift compensation was learnt and, if so, what sensory inputs underpinned it. We found that the effect of wind drift reduced significantly with both experience and access to visual landmark cues. Further, we found that the effect of experience on wind drift compensation was more pronounced when birds were out of sight of land. Our results suggest that improvement in wind drift compensation is not solely the product of either physical maturation or general improvements in flight control. Instead, we believe it is likely that they reflect how frigatebirds learn to process sensory information so as to reduce wind drift and maintain a constant course during goalward movement.

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.