Marked differences in foraging area use and susceptibility to predation between two closely-related tropical seabirds.

Ecological theory predicts that closely-related species must occupy different niches to coexist. How marine top predators achieve this during breeding, when they often gather in large multi-species colonies and are constrained to central-place foraging, has been mostly studied in productive temperate and polar oceans with abundant resources, but less so in poorer, tropical waters. Here, we track the foraging movements of two closely-related sympatric seabirds-the white-tailed and red-tailed tropicbirds Phaethon lepturus and P. rubricauda-breeding on Aldabra Atoll, Seychelles, to investigate potential mechanisms of niche segregation and shed light on their contrasting population trends. Combining data from GPS, immersion, depth and accelerometry loggers, we show that the two species have similar behaviour at sea, but are completely segregated spatially, with red-tailed tropicbirds flying further to feed and using different feeding areas than white-tailed tropicbirds. Using nest-based camera traps, we show that low breeding success of both species-which likely drives observed population declines-is caused by high nest predation. However, the two species are targeted by different predators, with native avian predators mainly targeting red-tailed tropicbird nests, and invasive rats raiding white-tailed tropicbird nests when they leave their eggs unattended. Our findings provide new insight into the foraging ecology of tropicbirds and have important conservation implications. The extensive range and spatial segregation highlight the importance of considering large-scale protection of waters around tropical seabird colonies, while the high level of nest predation provides evidence in support of rat eradication and investigating potential nest protection from native avian predators.

Evidence of tool use in a seabird.

Documenting novel cases of tool use in wild animals can inform our understanding of the evolutionary drivers of the behavior's emergence in the natural world. We describe a previously unknown tool-use behavior for wild birds, so far only documented in the wild in primates and elephants. We observed 2 Atlantic puffins at their breeding colonies, one in Wales and the other in Iceland (the latter captured on camera), spontaneously using a small wooden stick to scratch their bodies. The importance of these observations is 3-fold. First, while to date only a single form of body-care-related tool use has been recorded in wild birds (anting), our finding shows that the wild avian tool-use repertoire is wider than previously thought and extends to contexts other than food extraction. Second, we expand the taxonomic breadth of tool use to include another group of birds, seabirds, and a different suborder (Lari). Third, our independent observations span a distance of more than 1,700 km, suggesting that occasional tool use may be widespread in this group, and that seabirds' physical cognition may have been underestimated.

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.

A critical evaluation of the index of patch quality.

The inverse optimality approach can allow us to learn about an animal's environment by assuming their behaviour is optimal. This approach has been applied to animals diving underwater for food to produce the index of patch quality (IPQ), which aims to provide a proxy for prey abundance or quality in a foraging patch based on the animal's diving behaviour. The IPQ has been used in several empirical studies but has never been evaluated theoretically. Here, we discuss the strengths and weaknesses of the IPQ approach from a theoretical angle and review the empirical evidence supporting its use. We highlight several potential issues, in particular with the gain function-the function describing the energetic gain of an animal during a dive-used to calculate the IPQ. We investigate an alternative gain function which is appropriate in some cases, provide a new model based on this function, and discuss differences between the IPQ model and ours. We also find that there is little supporting empirical evidence justifying the general use of the IPQ and suggest future empirical validation methods which could help strengthen the case for the IPQ. Our findings have implications for the field of diving ecology and habitat assessment.

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.

Local prey shortages drive foraging costs and breeding success in a declining seabird, the Atlantic puffin.

As more and more species face anthropogenic threats, understanding the causes of population declines in vulnerable taxa is essential. However, long-term datasets, ideal to identify lasting or indirect effects on fitness measures such as those caused by environmental factors, are not always available. Here we use a single year but multi-population approach on populations with contrasting demographic trends to identify possible drivers and mechanisms of seabird population changes in the north-east Atlantic, using the Atlantic puffin, a declining species, as a model system. We combine miniature GPS trackers with camera traps and DNA metabarcoding techniques on four populations across the puffins' main breeding range to provide the most comprehensive study of the species' foraging ecology to date. We find that puffins use a dual foraging tactic combining short and long foraging trips in all four populations, but declining populations in southern Iceland and north-west Norway have much greater foraging ranges, which require more (costly) flight, as well as lower chick-provisioning frequencies, and a more diverse but likely less energy-dense diet, than stable populations in northern Iceland and Wales. Together, our findings suggest that the poor productivity of declining puffin populations in the north-east Atlantic is driven by breeding adults being forced to forage far from the colony, presumably because of low prey availability near colonies, possibly amplified by intraspecific competition. Our results provide valuable information for the conservation of this and other important North-Atlantic species and highlight the potential of multi-population approaches to answer important questions about the ecological drivers of population trends.

Exploration and refinement of migratory routes in long-lived birds.

In Focus: Campioni L., Dias M. P., Granadeiro J. P., & Catry P. (2019). An ontogenetic perspective on migratory strategy of a long-lived pelagic seabird: Timings and destinations change progressively during maturation. Journal of Animal Ecology, 89, 29-43. https://doi.org/10.1111/1365-2656.13044 How migration routes develop in long-lived migratory animals remains poorly understood. Campioni et al. (2019) tracked the migration of immature and breeding Cory's shearwaters and found that the timings and routes gradually changed with age. Young birds followed more exploratory routes at first, but gradually shortened and defined them as they matured, and they returned to the breeding grounds progressively earlier. These findings suggest that long-lived species start by exploring potentially suitable areas for the non-breeding season and progressively refine their migration route as they age.

Effects of age and reproductive status on individual foraging site fidelity in a long-lived marine predator.

Individual foraging specializations, where individuals use a small component of the population niche width, are widespread in nature with important ecological and evolutionary implications. In long-lived animals, foraging ability develops with age, but we know little about the ontogeny of individuality in foraging. Here we use precision global positioning system (GPS) loggers to examine how individual foraging site fidelity (IFSF), a common component of foraging specialization, varies between breeders, failed breeders and immatures in a long-lived marine predator-the northern gannet Morus bassanus Breeders (aged 5+) showed strong IFSF: they had similar routes and were faithful to distal points during successive trips. However, centrally placed immatures (aged 2-3) were far more exploratory and lacked route or foraging site fidelity. Failed breeders were intermediate: some with strong fidelity, others being more exploratory. Individual foraging specializations were previously thought to arise as a function of heritable phenotypic differences or via social transmission. Our results instead suggest a third alternative-in long-lived species foraging sites are learned during exploratory behaviours early in life, which become canalized with age and experience, and refined where possible-the exploration-refinement foraging hypothesis. We speculate similar patterns may be present in other long-lived species and moreover that long periods of immaturity may be a consequence of such memory-based individual foraging strategies.

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.

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.

Limited domestic introgression in a final refuge of the wild pigeon.

Domesticated animals have been culturally and economically important throughout history. Many of their ancestral lineages are extinct or genetically endangered following hybridization with domesticated relatives. Consequently, they have been understudied compared to the ancestral lineages of domestic plants. The domestic pigeon Columba livia, which was pivotal in Darwin's studies, has maintained outsized cultural significance. Its role as a model organism spans the fields of behavior, genetics, and evolution. Domestic pigeons have hybridized with their progenitor, the Rock Dove, rendering the latter of dubious genetic status. Here, we use genomic and morphological data from the putative Rock Doves of the British Isles to identify relictual undomesticated populations. We reveal that Outer Hebridean Rock Doves have experienced minimal levels of introgression. Our results outline the contemporary status of these wild pigeons, highlighting the role of hybridization in the homogenization of genetic lineages.

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.

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.

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.

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.

In Situ Clock Shift Reveals that the Sun Compass Contributes to Orientation in a Pelagic Seabird.

Compass orientation is central to the control of animal movement from the scale of local food-caching movements around a familiar area in parids [1] and corvids [2, 3] to the first autumn vector navigation of songbirds embarking on long-distance migration [4-6]. In the study of diurnal birds, where the homing pigeon, Columba livia, has been the main model, a time-compensated sun compass [7] is central to the two-step map-and-compass process of navigation from unfamiliar places, as well as guiding movement via a representation of familiar area landmarks [8-12]. However, its use by an actively navigating wild bird is yet to be shown. By phase shifting an animal's endogenous clock, known as clock-shifting [13-15], sun-compass use can be demonstrated when the animal incorrectly consults the sun's azimuthal position while homing after experimental displacement [15-17]. By applying clock-shift techniques at the nest of a wild bird during natural incubation, we show here that an oceanic navigator-the Manx shearwater, Puffinus puffinus-incorporates information from a time-compensated sun compass during homeward guidance to the breeding colony after displacement. Consistently with homing pigeons navigating within their familiar area [8, 9, 11, 18], we find that the effect of clock shift, while statistically robust, is partial in nature, possibly indicating the incorporation of guidance from landmarks into movement decisions.