Francis Daunt

Can Ethograms Be Automatically Generated Using Body Acceleration Data from Free-Ranging Birds?

An ethogram is a catalogue of discrete behaviors typically employed by a species. Traditionally animal behavior has been recorded by observing study individuals directly. However, this approach is difficult, often impossible, in the case of behaviors which occur in remote areas and/or at great depth or altitude. The recent development of increasingly sophisticated, animal-borne data loggers, has started to overcome this problem. Accelerometers are particularly useful in this respect because they can record the dynamic motion of a body in e.g. flight, walking, or swimming. However, classifying behavior using body acceleration characteristics typically requires prior knowledge of the behavior of free-ranging animals. Here, we demonstrate an automated procedure to categorize behavior from body acceleration, together with the release of a user-friendly computer application, “Ethographer”. We evaluated its performance using longitudinal acceleration data collected from a foot-propelled diving seabird, the European shag, Phalacrocorax aristotelis. The time series data were converted into a spectrum by continuous wavelet transformation. Then, each second of the spectrum was categorized into one of 20 behavior groups by unsupervised cluster analysis, using k-means methods. The typical behaviors extracted were characterized by the periodicities of body acceleration. Each categorized behavior was assumed to correspond to when the bird was on land, in flight, on the sea surface, diving and so on. The behaviors classified by the procedures accorded well with those independently defined from depth profiles. Because our approach is performed by unsupervised computation of the data, it has the potential to detect previously unknown types of behavior and unknown sequences of some behaviors.

The demographic impact of extreme events: stochastic weather drives survival and population dynamics in a long-lived seabird

1. Most scenarios for future climate change predict increased variability and thus increased frequency of extreme weather events. To predict impacts of climate change on wild populations, we need to understand whether this translates into increased variability in demographic parameters, which would lead to reduced population growth rates even without a change in mean parameter values. This requires robust estimates of temporal process variance, for example in survival, and identification of weather covariates linked to interannual variability. 2. The European shag Phalacrocorax aristotelis (L.) shows unusually large variability in population size, and large-scale mortality events have been linked to winter gales. We estimated first-year, second-year and adult survival based on 43 years of ringing and dead recovery data from the Isle of May, Scotland, using recent methods to quantify temporal process variance and identify aspects of winter weather linked to survival. 3. Survival was highly variable for all age groups, and for second-year and adult birds process variance declined strongly when the most extreme year was excluded. Survival in these age groups was low in winters with strong onshore winds and high rainfall. Variation in first-year survival was not related to winter weather, and process variance, although high, was less affected by extreme years. A stochastic population model showed that increasing process variance in survival would lead to reduced population growth rate and increasing probability of extinction. 4. As in other cormorants, shag plumage is only partially waterproof, presumably an adaptation to highly efficient underwater foraging. We speculate that this adaptation may make individuals vulnerable to rough winter weather, leading to boom-and-bust dynamics, where rapid population growth under favourable conditions allows recovery from periodic large-scale weather-related mortality. 5. Given that extreme weather events are predicted to become more frequent, species such as shags that are vulnerable to such events are likely to exhibit stronger reductions in population growth than would be expected from changes in mean climate. Vulnerability to extreme events thus needs to be accounted for when predicting the ecological impacts of climate change.

Telomere loss in relation to age and early environment in long-lived birds

Shortening of telomeres, specific nucleotide repeats that cap eukaryotic chromosomes, is thought to play an important role in cellular and organismal senescence. We examined telomere dynamics in two long–lived seabirds, the European shag and the wandering albatross. Telomere length in blood cells declines between the chick stage and adulthood in both species. However, among adults, telomere length is not related to age. This is consistent with reports of most telomere loss occurring early in life in other vertebrates. Thus, caution must be used in estimating annual rates of telomere loss, as these are probably not constant with age. We also measured changes within individuals in the wild, using repeat samples taken from individual shags as chicks and adults. We found high inter–individual variation in the magnitude of telomere loss, much of which was explained by circumstances during growth. Individuals laying down high tissue mass for their size showed greater telomere shortening. Independently of this, individuals born late in the season showed more telomere loss. Early conditions, possibly through their effects on oxidative stress, appear to play an important role in telomere attrition and thus potentially in the longevity of individuals.

Towards a climate-dependent paradigm of ammonia emission and deposition

Existing descriptions of bi-directional ammonia (NH3) land–atmosphere exchange incorporate temperature and moisture controls, and are beginning to be used in regional chemical transport models. However, such models have typically applied simpler emission factors to upscale the main NH3 emission terms. While this approach has successfully simulated the main spatial patterns on local to global scales, it fails to address the environment- and climate-dependence of emissions. To handle these issues, we outline the basis for a new modelling paradigm where both NH3 emissions and deposition are calculated online according to diurnal, seasonal and spatial differences in meteorology. We show how measurements reveal a strong, but complex pattern of climatic dependence, which is increasingly being characterized using ground-based NH3 monitoring and satellite observations, while advances in process-based modelling are illustrated for agricultural and natural sources, including a global application for seabird colonies. A future architecture for NH3 emission–deposition modelling is proposed that integrates the spatio-temporal interactions, and provides the necessary foundation to assess the consequences of climate change. Based on available measurements, a first empirical estimate suggests that 5°C warming would increase emissions by 42 per cent (28–67%). Together with increased anthropogenic activity, global NH3 emissions may increase from 65 (45–85) Tg N in 2008 to reach 132 (89–179) Tg by 2100.

Extrinsic and intrinsic determinants of winter foraging and breeding phenology in a temperate seabird

In temperate regions, winter presents animals with a number of challenges including depressed food abundance, increased daily energy requirements, higher frequency of extreme weather events and shortened day length. Overcoming these constraints is critical for overwintering survival and scheduling of future breeding of long-lived species and is likely to be state dependent, associated with intrinsic abilities such as food acquisition rates. We examined the relationship between environmental and intrinsic factors on overwintering foraging and subsequent breeding phenology of the European shag Phalacrocorax aristotelis, a diurnal marine predator. We tested a range of hypotheses relating to overwintering foraging time and location. We found that individuals greatly increased their foraging time in winter to a peak of more than 90% of available daylight at the winter solstice. The seasonal patterns of foraging time appear to be driven by a combination of light levels and weather conditions and may be linked to the availability of the shags principal prey, the lesser sandeel Ammodytes marinus. There was no evidence that shags dispersed south in winter to increase potential foraging time. Foraging time decreased after the winter solstice and, crucially, was correlated with subsequent breeding phenology, such that individuals that spent less time foraging in February bred earlier. The relationship was much stronger in females than males, in line with their more direct control of timing of breeding. Our results demonstrate that pre-breeding intrinsic foraging ability is critical in determining breeding phenology.

Seasonal interactions in the black-legged kittiwake, Rissa tridactyla: links between breeding performance and winter distribution

Relationships between events in one period of the annual cycle and behaviour in subsequent seasons are key determinants of individual life histories and population dynamics. However, studying such associations is challenging, given the difficulties in following individuals across seasons, particularly in migratory species. Relationships between breeding performance and subsequent winter ecology are particularly poorly understood, yet are likely to be profoundly important because of the costs of reproduction. Using geolocation technology, we show that black-legged kittiwakes that experienced breeding failure left their colony in southeast Scotland earlier than successful breeders. Moreover, a greater proportion of unsuccessful breeders (94% versus 53% successful) travelled over 3000 km to the West Atlantic, whereas fewer visited the East Atlantic (31% versus 80% successful), less than 1000 km from the colony. The two groups did not differ in the timing of return to the colony the following spring. However, 58 per cent of males made a previously undescribed long-distance pre-breeding movement to the central Atlantic. Our results demonstrate important links between reproductive performance and winter distribution, with significant implications for population dynamics. Furthermore, macro-scale segregation associated with breeding outcome is relevant to defining important wintering areas, in particular among declining species experiencing increasingly regular breeding failure.

Using behavioural and state variables to identify proximate causes of population change in a seabird

Changes in animal population size are driven by the interactions between intrinsic processes and extrinsic forces, and identifying the proximate mechanisms behind population change remains a fundamental question in ecology. Here we report on how measuring behavioural and state proxies of food availability among populations experiencing different growth rates can be used to rapidly identify proximate drivers of population trends. In recent decades, the Cape gannet Morus capensis has shown a major distributional shift with historically large colonies in Namibia decreasing rapidly, whilst numbers at South African colonies have increased, suggesting contrasting environmental conditions in the two regions. We compared per capita growth rates of five of the six extant colonies with foraging range (using miniaturised Global Positioning System loggers), foraging work rate, food delivery rates and body condition of breeding adults. We found significant associations between the rate of population change, individual behaviour, energetic gain and body condition that indicate that recent population changes are associated with extrinsic effects. This study shows that behavioural and state data can be used to identify important drivers of population change, and their cost-effectiveness ensures that they are an appealing option for measuring the health of animal populations in numerous situations.

Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird

Exposure to stressors early in life is associated with faster ageing and reduced longevity. One important mechanism that could underlie these late life effects is increased telomere loss. Telomere length in early post-natal life is an important predictor of subsequent lifespan, but the factors underpinning its variability are poorly understood. Recent human studies have linked stress exposure to increased telomere loss. These studies have of necessity been non-experimental and are consequently subjected to several confounding factors; also, being based on leucocyte populations, where cell composition is variable and some telomere restoration can occur, the extent to which these effects extend beyond the immune system has been questioned. In this study, we experimentally manipulated stress exposure early in post-natal life in nestling European shags (Phalacrocorax aristotelis) in the wild and examined the effect on telomere length in erythrocytes. Our results show that greater stress exposure during early post-natal life increases telomere loss at this life-history stage, and that such an effect is not confined to immune cells. The delayed effects of increased telomere attrition in early life could therefore give rise to a ‘time bomb’ that reduces longevity in the absence of any obvious phenotypic consequences early in life.

From cradle to early grave: juvenile mortality in European shags Phalacrocorax aristotelis results from inadequate development of foraging proficiency

In most long-lived animal species, juveniles survive less well than adults. A potential mechanism is inferior foraging skills but longitudinal studies that follow the development of juvenile foraging are needed to test this. We used miniaturized activity loggers to record daily foraging times of juvenile and adult European shags Phalacrocorax aristotelis from fledging to the following spring. Juveniles became independent from their parents 40 days post-fledging. They compensated for poor foraging proficiency by foraging for approximately 3 h d−1 longer than adults until constrained by day length in early November. Thereafter, juvenile foraging time tracked shortening day length up to the winter solstice, when foraging time of the two age classes converged and continued to track day length until early February. Few individuals died until midwinter and mortality peaked in January–February, with juvenile mortality (including some of the study birds) five times that of adults. In their last two weeks of life, juveniles showed a marked decline in foraging time consistent with individuals becoming moribund. Our results provide compelling evidence that juveniles compensate for poor foraging proficiency by increasing foraging time, a strategy that is limited by day length resulting in high winter mortality.

Regulation of stroke and glide in a foot-propelled avian diver.

SUMMARY Bottom-feeding, breath-hold divers would be expected to minimize transit time between the surface and foraging depth, thus maximizing the opportunities for prey capture during the bottom phase of the dive. To achieve this they can potentially adjust a variety of dive parameters, including dive angle and swim speed. However, because of predictable changes in buoyancy with depth, individuals would also be expected to adjust dive behavior according to dive depth. To test these predictions we deployed miniature, dorsally attached data-loggers that recorded surge and heave accelerations at 64 Hz to obtain the first detailed measurements of a foot-propelled diving bird, the European shag Phalacrocorax aristotelis, in the wild. The results were used to investigate biomechanical changes during the descent, ascent and bottom phases for dives varying between 7 m and 43 m deep. Shags descended and ascended almost vertically (60–90° relative to the sea surface). During descent, swim speed varied between 1.2–1.8 m s–1 and the frequency of the foot stroke used for propulsion decreased significantly with depth, mainly due to a fivefold increase in the duration of the glide between strokes. Birds appeared to maintain the duration and the maximum strength of power stroke and thus optimize muscle contraction efficiency.