Population ecology and conservation of red-billed choughs in Scotland. Final report on Knowledge Transfer Project

This report summarises the results of a Knowledge Transfer Research Project that was undertaken by Dr Jane Reid (University of Aberdeen), Professor Pat Monaghan, (University of Glasgow), Dr Eric and Mrs Sue Bignal (Scottish Chough Study Group) and Dr Davy McCracken (Scottish Agricultural College). Dr Maria Bogdanova was employed as the postdoctoral research assistant on the project. The work was carried out in partnership with Scottish Natural Heritage (SNH) and the Royal Society for the Protection of Birds (RSPB). Funding was provided by a Knowledge Transfer Grant from the Natural Environment Research Council (NERC, PIs P. Monaghan & J. Reid), with matching partnership funding and in-kind support from SNH and RSPB. The overall aims of the project were to develop the scientific understanding of the population ecology of choughs on Islay, and to use this understanding to inform the development of appropriate conservation strategies and policies. The project built on existing long-term research on Islay’s choughs. It involved further analysis of long-term data, plus two years of intensive fieldwork designed to answer specific questions. The work aimed primarily to understand the ecology of choughs in their sub-adult years (ie, from fledging to breeding age). Survival from fledging to breeding is a key factor in causing population change. However, relatively little was previously known about the behaviour and ecology of choughs during this time. This report provides an overview of the results of the scientific study and focuses on presenting the scientific evidence on which resulting recommendations for chough conservation management on Islay are based. The report is written with the intention of presenting the results of the data analyses, and the rationale underlying those analyses, in a way that is accessible to non-specialists. Further details of analyses and technicalities are provided in published, peer-reviewed papers and/or are available on request. The report provides information that will be of use to policy makers and conservation practitioners, and also highlights topics where further research is required before informed management decisions can be taken

Among-year and within-population variation in foraging distribution of European shags Phalacrocorax aristotelis over two decades: implications for marine spatial planning

Marine spatial planning aims to deliver sustainable use of marine resources by minimizing environmental impacts of human activities and designating Marine Protected Areas. This poses a challenge where species’ distributions show spatio-temporal heterogeneity. However, due to logistic constraints and challenging timescales many studies of distribution are undertaken over few years or on a restricted subset of the population. Long-term studies can help identify the degree of uncertainty in those less comprehensive in space and time. We quantify inter-annual and sub-colony variation in the summer foraging distribution of a population of European shags Phalacrocorax aristotelis, using a tracking data set comprising 320 individuals and 1106 foraging trips in 15 years from 1987 to 2010. Foraging distribution over the study period was concentrated in three areas. Data from one and two years captured an average of 54% and 64% of this distribution, respectively, but it required 8 years’ data to capture over 90% of the distribution. Foraging range increased with population size when breeding success was low, suggesting interplay between extrinsic and intrinsic effects. Furthermore, females had foraging ranges on average 36% greater than males. Finally, sub-colony segregation occurred in foraging areas up to 4 km from the colony and in the most distant locations (>10 km), whilst there was considerable overlap at intermediate distances (6–10 km). Our study highlights important considerations for marine spatial planning in particular, and species conservation in general, notably the proportion of the population distribution identified, the prevailing conditions experienced and the need for balanced sampling across the population

Modelling and mapping how common guillemots balance their energy budgets over a full annual cycle

The ability of individual animals to balance their energy budgets throughout the annual cycle is important for their survival, reproduction and population dynamics. However, the annual cycles of many wild, mobile animals are difficult to observe and our understanding of how individuals balance their energy budgets throughout the year therefore remains poor. We developed a hierarchical Bayesian state-space model to investigate how key components of animal energy budgets (namely individual energy gain and storage) varied in space and time. Our model used biologger-derived estimates of time-activity budgets, locations and energy expenditure to infer year-round time series of energy income and reserves. The model accounted for seasonality in environmental drivers such as sea surface temperature and daylength, allowing us to identify times and locations of high energy gain. Our study system was a population of common guillemots Uria aalge breeding at a western North Sea colony. These seabirds manage their energy budgets by adjusting their behaviour and accumulating fat reserves. However, typically during severe weather conditions, birds can experience an energy deficit over a sustained period, leading to starvation and large-scale mortality events. We show that guillemot energy gain varied in both time and space. Estimates of guillemot body mass varied throughout the annual cycle and birds periodically experienced losses in mass. Mass losses were likely to have either been adaptive, or due to energetic bottlenecks, the latter leading to increased susceptibility to mortality. Guillemots tended to be lighter towards the edge of their spatial distribution. We describe a framework that combines biologging data, time-activity budget analysis and Bayesian state-space modelling to identify times and locations of high energetic reward or potential energetic bottlenecks in a wild animal population. Our approach can be extended to address ecological and conservation-driven questions that were previously unanswerable due to logistical complexities in collecting data on wild, mobile animals across full annual cycles

Opposing effects of spatiotemporal variation in resources and temporal variation in climate on density dependent population growth in seabirds

1. Understanding how ecological processes combine to shape population dynamics is crucial in a rapidly changing world. Evidence has been emerging for how fundamental drivers of density dependence in mobile species are related to two differing types of environmental variation—temporal variation in climate, and spatiotemporal variation in food resources. However, to date, tests of these hypotheses have been largely restricted to mid-trophic species in terrestrial environments and thus their general applicability remains unknown. 2. We tested if these same processes can be identified in marine upper trophic level species. We assembled a multi-decadal data set on population abundance of 10 species of colonial seabirds comprising a large component of the UK breeding seabird biomass, and covering diverse phylogenies, life histories and foraging behaviours. 3. We tested for evidence of density dependence in population growth rates using discrete time state-space population models fit to long time-series of observations of abundance at seabird breeding colonies. We then assessed if the strength of density dependence in population growth rates was exacerbated by temporal variation in climate (sea temperature and swell height), and attenuated by spatiotemporal variation in prey resources (productivity and tidal fronts). 4. The majority of species showed patterns consistent with temporal variation in climate acting to strengthen density dependent feedbacks to population growth. However, fewer species showed evidence for a weakening of density dependence with increasing spatiotemporal variation in prey resources. 5. Our findings extend this emerging theory for how different sources of environmental variation may shape the dynamics and regulation of animal populations, demonstrating its role in upper trophic marine species. We show that environmental variation leaves a signal in long-term population dynamics of seabirds with potentially important consequences for their demography and trophic interactions

Multi-colony tracking reveals spatio-temporal variation in carry-over effects between breeding success and winter movements in a pelagic seabird

Carry-over effects, whereby events in one season have consequences in subsequent seasons, have important demographic implications. Although most studies examine carry-over effects across 2 seasons in single populations, the effects may persist beyond the following season and vary across a species’ range. To assess potential carry-over effects across the annual cycle and among populations, we deployed geolocation loggers on black-legged kittiwakes Rissa tridactyla at 10 colonies in the north-east Atlantic and examined relationships between the timing and destination of migratory movements and breeding success in the year of deployment and subsequent season. Both successful and unsuccessful breeders wintered primarily in the north-west Atlantic. Breeding success affected the timing of migration, whereby unsuccessful breeders departed the colony earlier, arrived at the post-breeding and main wintering areas sooner, and departed later the following spring. However, these patterns were only apparent in colonies in the south-west of the study region. Furthermore, the effect of breeding success was stronger on migration timing in the first part of the winter than later. Timing of migratory movements was weakly linked to subsequent breeding success, and there was no detectable association between breeding success in the 2 seasons. Our results indicate temporal structure and spatial hetero - geneity in the strength of seasonal interactions among kittiwakes breeding in the north-east Atlantic. Variable fitness consequences for individuals from different colonies could have important implications for population processes across the species’ range and suggest that the spatio-temporal dynamics of carry-over effects warrant further study

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

Quantifying annual spatial consistency in chick-rearing seabirds to inform important site identification

Animal tracking has afforded insights into patterns of space use in numerous species and thereby informed area-based conservation planning. A crucial consideration when estimating spatial distributions from tracking data is whether the sample of tracked animals is representative of the wider population. However, it may also be important to track animals in multiple years to capture changes in distribution in response to varying environmental conditions. Using GPS-tracking data from 23 seabird species, we assessed the importance of multi-year sampling for identifying important sites for conservation during the chick-rearing period, when seabirds are most spatially constrained. We found a high degree of spatial overlap among distributions from different years in most species. Multi-year sampling often captured a significantly higher portion of reference distributions (based on all data for a population) than sampling in a single year. However, we estimated that data from a single year would on average miss only 5 % less of the full distribution of a population compared to equal-sized samples collected across three years (min: −0.3 %, max: 17.7 %, n = 23). Our results suggest a key consideration for identifying important sites from tracking data is whether enough individuals were tracked to provide a representative estimate of the population distribution during the sampling period, rather than that tracking necessarily take place in multiple years. By providing an unprecedented multi-species perspective on annual spatial consistency, this work has relevance for the application of tracking data to informing the conservation of seabirds

The FANCM:p.Arg658* truncating variant is associated with risk of triple-negative breast cancer.

Breast cancer is a common disease partially caused by genetic risk factors. Germline pathogenic variants in DNA repair genes BRCA1, BRCA2, PALB2, ATM, and CHEK2 are associated with breast cancer risk. FANCM, which encodes for a DNA translocase, has been proposed as a breast cancer predisposition gene, with greater effects for the ER-negative and triple-negative breast cancer (TNBC) subtypes. We tested the three recurrent protein-truncating variants FANCM:p.Arg658*, p.Gln1701*, and p.Arg1931* for association with breast cancer risk in 67,112 cases, 53,766 controls, and 26,662 carriers of pathogenic variants of BRCA1 or BRCA2. These three variants were also studied functionally by measuring survival and chromosome fragility in FANCM -/- patient-derived immortalized fibroblasts treated with diepoxybutane or olaparib. We observed that FANCM:p.Arg658* was associated with increased risk of ER-negative disease and TNBC (OR = 2.44, P = 0.034 and OR = 3.79; P = 0.009, respectively). In a country-restricted analysis, we confirmed the associations detected for FANCM:p.Arg658* and found that also FANCM:p.Arg1931* was associated with ER-negative breast cancer risk (OR = 1.96; P = 0.006). The functional results indicated that all three variants were deleterious affecting cell survival and chromosome stability with FANCM:p.Arg658* causing more severe phenotypes. In conclusion, we confirmed that the two rare FANCM deleterious variants p.Arg658* and p.Arg1931* are risk factors for ER-negative and TNBC subtypes. Overall our data suggest that the effect of truncating variants on breast cancer risk may depend on their position in the gene. Cell sensitivity to olaparib exposure, identifies a possible therapeutic option to treat FANCM-associated tumors

Energetic synchrony throughout the non-breeding season in common guillemots from four colonies

The non‐breeding season presents significant energetic challenges to birds that breed in temperate or polar regions, with clear implications for population dynamics. In seabirds, the environmental conditions at non‐breeding sites drive food availability and the energetic cost of regulatory processes, resulting in variation in diet, behaviour and energetics; however, very few studies have attempted to understand if and how these aspects vary between populations. We investigated whether non‐breeding location influenced diet, behaviour and energetics in the common guillemot Uria aalge. We studied guillemots from four UK breeding colonies, two located on the west coast of Scotland and two on the east. We quantified non‐breeding distribution, foraging behaviour and activity budgets of 39 individuals from July to March, using geolocation–immersion loggers and time‐depth recorders, and used feather stable isotope signatures to infer diet during the post‐breeding moult. We calculated energy expenditure and investigated whether the peak (an indicator of the potential vulnerability to marine threats) varied between colonies. Individuals were spatially segregated according to the coastline they breed on, with west coast guillemots distributed off the west coast of the UK and east coast guillemots distributed off the east coast. Diet and behaviour were more similar in guillemots that shared a breeding coastline than those that did not, as west coast guillemots foraged at a lower trophic level, spent less time diving and engaged in more pelagic foraging than east coast guillemots. However, energy expenditure was remarkably similar between colonies, peaking during late February/early March, indicating that, during our study period, there was high synchrony between colonies in the timing of potential vulnerability to marine threats. Therefore, any anthropogenic changes that result in decreased food availability or increased energy expenditure during late winter may have greater impacts on energy balance, with consequences for population dynamics.</jats:p