Seabirds show foraging site and route fidelity but demonstrate flexibility in response to local information.

BACKGROUND: Fidelity to a given foraging location or route may be beneficial when environmental conditions are predictable but costly if conditions deteriorate or become unpredictable. Understanding the magnitude of fidelity displayed by different species and the processes that drive or erode it is therefore vital for understanding how fidelity may shape the demographic consequences of anthropogenic change. In particular, understanding the information that individuals may use to adjust their fidelity will facilitate improved predictions of how fidelity may change as environments change and the extent to which it will buffer individuals against such changes. METHODS: We used movement data collected during the breeding season across eight years for common guillemots, Atlantic puffins, razorbills, and black-legged kittiwakes breeding on the Isle of May, Scotland to understand: (1) whether foraging site/route fidelity occurred within and between years, (2) whether the degree of fidelity between trips was predicted by personal foraging effort, and (3) whether different individuals made more similar trips when they overlapped in time at the colony prior to departure and/or when out at sea suggesting the use of the same local environmental cues or information on the decisions made by con- and heterospecifics. RESULTS: All species exhibited site and route fidelity both within- and between-years, and fidelity between trips in guillemots and razorbills was related to metrics of foraging effort, suggesting they adjust fidelity to their personal foraging experience. We also found evidence that individuals used local environmental cues of prey location or availability and/or information gained by observing conspecifics when choosing foraging routes, particularly in puffins, where trips of individuals that overlapped temporally at the colony or out at sea were more similar. CONCLUSIONS: The fidelity shown by these seabird species has the potential to put them at greater risk in the face of environmental change by driving individuals to continue using areas being degraded by anthropogenic pressures. However, our results suggest that individuals show some flexibility in their fidelity, which may promote resilience under environmental change. The benefits of this flexibility are likely to depend on numerous factors, including the rapidity and spatial scale of environmental change and the reliability of the information individuals use to choose foraging sites or routes, thus highlighting the need to better understand how organisms combine cues, prior experience, and other sources of information to make movement decisions.

Consequences of cross-season demographic correlations for population viability.

Demographic correlations are pervasive in wildlife populations and can represent important secondary drivers of population growth. Empirical evidence suggests that correlations are in general positive for long-lived species, but little is known about the degree of variation among spatially segregated populations of the same species in relation to environmental conditions. We assessed the relative importance of two cross-season correlations in survival and productivity, for three Atlantic puffin (Fratercula arctica) populations with contrasting population trajectories and non-overlapping year-round distributions. The two correlations reflected either a relationship between adult survival prior to breeding on productivity, or a relationship between productivity and adult survival the subsequent year. Demographic rates and their correlations were estimated with an integrated population model, and their respective contributions to variation in population growth were calculated using a transient-life table response experiment. For all three populations, demographic correlations were positive at both time lags, although their strength differed. Given the different year-round distributions of these populations, this variation in the strength population-level demographic correlations points to environmental conditions as an important driver of demographic variation through life-history constraints. Consequently, the contributions of variances and correlations in demographic rates to population growth rates differed among puffin populations, which has implications for-particularly small-populations' viability under environmental change as positive correlations tend to reduce the stochastic population growth rate.

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.

Earlier and more frequent occupation of breeding sites during the non-breeding season increases breeding success in a colonial seabird.

Competition for high-quality breeding sites in colonial species is often intense, such that individuals may invest considerable time in site occupancy even outside the breeding season. The site defense hypothesis predicts that high-quality sites will be occupied earlier and more frequently, consequently those sites will benefit from earlier and more successful breeding. However, few studies relate non-breeding season occupancy to subsequent breeding performance limiting our understanding of the potential life-history benefits of this behavior. Here, we test how site occupancy in the non-breeding season related to site quality, breeding timing, and breeding success in a population of common guillemots Uria aalge, an abundant and well-studied colonially breeding seabird. Using time-lapse photography, we recorded occupancy at breeding sites from October to March over three consecutive non-breeding seasons. We then monitored the successive breeding timing (lay date) and breeding success at each site. On average, sites were first occupied on the 27th October ± 11.7 days (mean ± SD), subsequently occupied on 46 ± 18% of survey days and for 55 ± 15% of the time when at least one site was occupied. Higher-quality sites, sites with higher average historic breeding success, were occupied earlier, more frequently and for longer daily durations thereafter. Laying was earlier at sites that were occupied more frequently and sites occupied earlier were more successful, supporting the site defense hypothesis. A path analysis showed that the return date had a greater or equal effect on breeding success as lay date. Pair level occupancy had no effect on breeding timing or success. The clear effect of non-breeding occupancy of breeding sites on breeding timing and success highlights the benefits of this behavior on demography in this population and the importance of access to breeding sites outside the breeding season in systems where competition for high-quality sites is intense.

Complex population structure of the Atlantic puffin revealed by whole genome analyses.

The factors underlying gene flow and genomic population structure in vagile seabirds are notoriously difficult to understand due to their complex ecology with diverse dispersal barriers and extensive periods at sea. Yet, such understanding is vital for conservation management of seabirds that are globally declining at alarming rates. Here, we elucidate the population structure of the Atlantic puffin (Fratercula arctica) by assembling its reference genome and analyzing genome-wide resequencing data of 72 individuals from 12 colonies. We identify four large, genetically distinct clusters, observe isolation-by-distance between colonies within these clusters, and obtain evidence for a secondary contact zone. These observations disagree with the current taxonomy, and show that a complex set of contemporary biotic factors impede gene flow over different spatial scales. Our results highlight the power of whole genome data to reveal unexpected population structure in vagile marine seabirds and its value for seabird taxonomy, evolution and conservation.

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.

Reproductive performance of resident and migrant males, females and pairs in a partially migratory bird.

Quantifying among-individual variation in life-history strategies, and associated variation in reproductive performance and resulting demographic structure, is key to understanding and predicting population dynamics and life-history evolution. Partial migration, where populations comprise a mixture of resident and seasonally migrant individuals, constitutes a dimension of life-history variation that could be associated with substantial variation in reproductive performance. However, such variation has rarely been quantified due to the challenge of measuring reproduction and migration across a sufficient number of seasonally mobile males and females. We used intensive winter (non-breeding season) resightings of colour-ringed adult European shags (Phalacrocorax aristotelis) from a known breeding colony to identify resident and migrant individuals. We tested whether two aspects of annual reproductive performance, brood hatch date and breeding success, differed between resident and migrant males, females and breeding pairs observed across three consecutive winters and breeding seasons. The sex ratios of observed resident and migrant shags did not significantly differ from each other or from 1:1, suggesting that both sexes are partially migratory and that migration was not sex-biased across surveyed areas. Individual resident males and females hatched their broods 6 days earlier and fledged 0.2 more chicks per year than migrant males and females on average. Resident individuals of both sexes therefore had higher breeding success than migrants. Hatch date and breeding success also varied with a pair's joint migratory strategy such that resident-resident pairs hatched their broods 12 days earlier than migrant-migrant pairs, and fledged 0.7 more chicks per year on average. However, there was no evidence of assortative pairing with respect to migratory strategy: observed frequencies of migrant-migrant and resident-resident pairs did not differ from those expected given random pairing. These data demonstrate substantial variation in two key aspects of reproductive performance associated with the migratory strategies of males, females and breeding pairs within a partially migratory population. These patterns could reflect direct and/or indirect mechanisms, but imply that individual variation in migratory strategy and variation in pairing among residents and migrants could influence selection on migration and drive complex population and evolutionary dynamics.

Investigating the effects of age-related spatial structuring on the transmission of a tick-borne virus in a colonially breeding host.

Higher pathogen and parasite transmission is considered a universal cost of colonial breeding due to the physical proximity of colony members. However, this has rarely been tested in natural colonies, which are structured entities, whose members interact with a subset of individuals and differ in their infection histories. We use a population of common guillemots, Uria aalge, infected by a tick-borne virus, Great Island virus, to explore how age-related spatial structuring can influence the infection costs borne by different members of a breeding colony. Previous work has shown that the per-susceptible risk of infection (force of infection) is different for prebreeding (immature) and breeding (adult) guillemots which occupy different areas of the colony. We developed a mathematical model which showed that this difference in infection risk can only be maintained if mixing between these age groups is low. To estimate mixing between age groups, we recorded the movements of 63 individually recognizable, prebreeding guillemots in four different parts of a major colony in the North Sea during the breeding season. Prebreeding guillemots infrequently entered breeding areas (in only 26% of watches), though with marked differences in frequency of entry among individuals and more entries toward the end of the breeding season. Once entered, the proportion of time spent in breeding areas by prebreeding guillemots also varied between different parts of the colony. Our data and model predictions indicate low levels of age-group mixing, limiting exposure of breeding guillemots to infection. However, they also suggest that prebreeding guillemots have the potential to play an important role in driving infection dynamics. This highlights the sensitivity of breeding colonies to changes in the behavior of their members-a subject of particular importance in the context of global environmental change.

Site fidelity and individual variation in winter location in partially migratory European shags.

In partially migratory populations, individuals from a single breeding area experience a range of environments during the non-breeding season. If individuals show high within- and among- year fidelity to specific locations, any annual environmental effect on individual life histories could be reinforced, causing substantial demographic heterogeneity. Quantifying within- and among- individual variation and repeatability in non-breeding season location is therefore key to predicting broad-scale environmental impacts on the dynamics of partially migratory populations. We used field resightings of colour-ringed adult European shags known to have bred on the Isle of May, Scotland, to quantify individual variation and repeatability in winter location within and among three consecutive winters. In total, 3797 resightings of 882 individuals were recorded over 622 km of coastline, including the Isle of May. These individuals comprised over 50% of the known breeding population, and encompassed representative distributions of ages and sexes. The distances from the Isle of May at which individuals were resighted during winter varied substantially, up to 486 km and 136 km north and south respectively and including the breeding colony on the Isle of May. However, resighting distances were highly repeatable within individuals; within- and among-winter repeatabilities were >0.72 and >0.59 respectively across the full September-March observation period, and >0.95 and >0.79 respectively across more restricted mid-winter periods. Repeatability did not differ significantly between males and females or among different age classes, either within or among winters. These data demonstrate that the focal shag population is partially migratory, and moreover that individuals show highly repeatable variation in winter location and hence migration strategy across consecutive winters. Such high among-individual variation and within-individual repeatability, both within and among winters, could lead to substantial life history variation, and therefore influence population dynamics and future conservation management strategies.

Modelling the effects of prey size and distribution on prey capture rates of two sympatric marine predators.

Understanding how prey capture rates are influenced by feeding ecology and environmental conditions is fundamental to assessing anthropogenic impacts on marine higher predators. We compared how prey capture rates varied in relation to prey size, prey patch distribution and prey density for two species of alcid, common guillemot (Uria aalge) and razorbill (Alca torda) during the chick-rearing period. We developed a Monte Carlo approach parameterised with foraging behaviour from bird-borne data loggers, observations of prey fed to chicks, and adult diet from water-offloading, to construct a bio-energetics model. Our primary goal was to estimate prey capture rates, and a secondary aim was to test responses to a set of biologically plausible environmental scenarios. Estimated prey capture rates were 1.5 ± 0.8 items per dive (0.8 ± 0.4 and 1.1 ± 0.6 items per minute foraging and underwater, respectively) for guillemots and 3.7 ± 2.4 items per dive (4.9 ± 3.1 and 7.3 ± 4.0 items per minute foraging and underwater, respectively) for razorbills. Based on species' ecology, diet and flight costs, we predicted that razorbills would be more sensitive to decreases in 0-group sandeel (Ammodytes marinus) length (prediction 1), but guillemots would be more sensitive to prey patches that were more widely spaced (prediction 2), and lower in prey density (prediction 3). Estimated prey capture rates increased non-linearly as 0-group sandeel length declined, with the slope being steeper in razorbills, supporting prediction 1. When prey patches were more dispersed, estimated daily energy expenditure increased by a factor of 3.0 for guillemots and 2.3 for razorbills, suggesting guillemots were more sensitive to patchier prey, supporting prediction 2. However, both species responded similarly to reduced prey density (guillemot expenditure increased by 1.7; razorbill by 1.6), thus not supporting prediction 3. This bio-energetics approach complements other foraging models in predicting likely impacts of environmental change on marine higher predators dependent on species-specific foraging ecologies.

Impacts of poor food availability on positive density dependence in a highly colonial seabird.

For species with positive density dependence, costs and benefits of increasing density may depend on environmental conditions, but this has seldom been tested. By examining a colonial seabird (common guillemot) over a period of unprecedented poor food availability, we test two contrasting hypotheses suggesting that birds breeding at high density have: (i) greater leeway to increase foraging effort owing to more effective defence of unattended chicks against predators; and (ii) less leeway, owing to more attacks on unattended chicks by neighbouring adults. Supporting hypothesis 1, birds at high density increased provisioning rates and hence survival of chicks by foraging simultaneously with their partners, whereas at low density, unattended chicks were liable to be killed by predatory gulls and, unexpectedly, razorbills. Simultaneously, supporting hypothesis 2, heightened aggression towards unattended chicks at high density frequently resulted in infanticide, undermining benefits from collective defence against predators. Consequently, over 25 years, the magnitude of positive density dependence was independent of mean breeding success. These data indicate previously unsuspected trade-offs between costs and benefits of increasing density under changing environments. Previous generalizations about the importance of high density for reproductive success have so far remained robust, but such trade-offs could have unpredictable consequences for future population dynamics.

Hitting the buffers: conspecific aggression undermines benefits of colonial breeding under adverse conditions.

Colonial breeding in birds is widely considered to benefit individuals through enhanced protection against predators or transfer of information about foraging sites. This view, however, is largely based on studies of seabirds carried out under favourable conditions. Recent breeding failures at many seabird colonies in the UK provide an opportunity to re-examine costs and benefits of coloniality under adverse conditions. Common guillemots Uria aalge are highly colonial cliff-nesting seabirds with very flexible parental care. Although the single chick is normally never left alone, more than 50 per cent of offspring were left unattended at a North Sea colony in 2007, apparently because poor conditions forced both parents to forage simultaneously. Contrary to expectation, unattended chicks were not killed by avian predators. Rather, although non-breeders and failed breeders sometimes provided alloparental care, unattended chicks were frequently attacked by breeding guillemots at neighbouring sites, often with fatal consequences. These results highlight a previously unsuspected trade-off between provisioning chicks and avoiding conspecific attacks, and indicate that understanding how environmental conditions affect social dynamics is crucial to interpreting costs and benefits of colonial breeding.

Fitness increases with partner and neighbour allopreening.

Altruism and selfishness are fundamental characteristics of human and animal societies. Among colonial biparental species, breeding outcome depends on interactions between mates and neighbours. However, the relationships between cooperation within and among partnerships and fitness have not been fully investigated. We show that in the highly colonial common guillemot (Uria aalge), altruistic behaviour (allopreening) towards a mate was positively related to long-term fitness, whereas allopreening a neighbour was related to current fitness. Turnover is much lower within than between pairs, so our results suggest that allopreening within pairs generates fitness returns at longer timescales than between pairs. Allopreening not only removes ectoparasites and maintains plumage condition, but may also have important social functions. We found a negative relationship between fight rate and allopreen rate between breeding neighbours, with nests exhibiting low breeding success having a higher frequency of fights with neighbours. We also found evidence for reciprocity in allopreening. Thus, allopreening may function as a reciprocal stress reducer, to decrease the likelihood of fights and associated breeding failure. We suggest that altruistic behaviour has long-term benefits for the survival of the offspring when living in a crowded neighbourhood.

Determinants of quality in a long-lived colonial species.

1. In many animal populations a small proportion of individuals produce the majority of surviving offspring, but the underlying mechanisms are unclear. Behaviour may be an important determinant of variation in fitness: 'high-quality' individuals may have enhanced abilities in foraging or predator and parasite avoidance. 2. The role of behaviour in determining variation in quality was examined using the common guillemot Uria aalge, a monogamous seabird with biparental care. Using a novel mixed model approach, we analysed binary data on breeding success of each pair attempting to breed in each year with variables critical to breeding success (timing of breeding; inferred age; breeding experience and success; number of nest sites and partners) as fixed effects. Random effects for year, male, female and each distinct pairing of a male and a female were included in the model, allowing a quality estimate to be derived for each individual and pair. A range of behaviours associated with breeding were examined in relation to these quality estimates. 3. Breeding success declined with timing of breeding, and increased initially with age before declining in old age. It increased with previous successful experience, not breeding experience per se, until senescence effects became apparent. For males, breeding success declined with increasing numbers of mates. 4. The most important behavioural determinants of quality operated at the level of the pair, with the time mates spent together at the site and chick feeding rates both positively related to quality. At the individual level, trip durations and feeding rates were associated with female but not male quality, suggesting that pair quality was operating principally through the female. However, removal of laying date, the most important component in the binomial model, confirmed that the pair effect was much larger than the female effect. 5. This study demonstrates the potential of mixed modelling to determine quality estimates based on long-term breeding histories. The probability of a successful reproductive attempt was explained by the timing of breeding, age, successful breeding experience and number of mates. Behaviour was an important proximate mechanism underlying quality, in particular the foraging abilities of the pair, and the female's contribution to offspring provisioning. In species with biparental care, behavioural correlates of quality operate most strongly at the scale of the breeding pair, because contributions from both individuals are required for a successful outcome.