Hemispheric asymmetry in ocean change and the productivity of ecosystem sentinels.

Climate change and other human activities are causing profound effects on marine ecosystem productivity. We show that the breeding success of seabirds is tracking hemispheric differences in ocean warming and human impacts, with the strongest effects on fish-eating, surface-foraging species in the north. Hemispheric asymmetry suggests the need for ocean management at hemispheric scales. For the north, tactical, climate-based recovery plans for forage fish resources are needed to recover seabird breeding productivity. In the south, lower-magnitude change in seabird productivity presents opportunities for strategic management approaches such as large marine protected areas to sustain food webs and maintain predator productivity. Global monitoring of seabird productivity enables the detection of ecosystem change in remote regions and contributes to our understanding of marine climate impacts on ecosystems.

Longitudinal bio-logging reveals interplay between extrinsic and intrinsic carry-over effects in a long-lived vertebrate.

Carry-over effects have major implications for individual fitness and population and evolutionary dynamics. The strength of these effects is dependent on an individual's intrinsic performance and the environmental conditions it experiences. However, understanding the relative importance of environmental and intrinsic effects underpinning seasonal interactions has proved extremely challenging, since they covary. A powerful approach is longitudinal measurement of individuals across a range of conditions, whereby each animal is effectively acting as its own control. We related time spent foraging during the nonbreeding period to subsequent breeding performance in European Shags Phalacrocorax aristotelis. By following individuals for up to six years, we could test simultaneously for extrinsic and intrinsic effects using random regression modeling. We detected significant annual and among-individual variation in daily foraging time during the late winter, and clear variation among individuals in the quadratic relationship between foraging time and date. Shorter foraging times were associated with earlier and more successful breeding, driven by differences among years and individuals, with no evidence of individual variation in the slope of these relationships. That both environmental and intrinsic variation shape carry-over effects has important implications for population responses to environmental change.

Influence of wing loading on the trade-off between pursuit-diving and flight in common guillemots and razorbills.

Species of bird that use their wings for underwater propulsion are thought to face evolutionary trade-offs between flight and diving, leading to the prediction that species with different wing areas relative to body mass (i.e. different wing loadings) also differ in the relative importance of flight and diving activity during foraging trips. We tested this hypothesis for two similarly sized species of Alcidae (common guillemots and razorbills) by using bird-borne devices to examine three-dimensional foraging behaviour at a single colony. Guillemots have 30% higher wing loading than razorbills and, in keeping with this difference, razorbills spent twice as long in flight as a proportion of trip duration whereas guillemots spent twice as long in diving activity. Razorbills made a large number of short, relatively shallow dives and spent little time in the bottom phase of the dive whereas guillemots made fewer dives but frequently attained depths suggesting that they were near the seabed (ca. 35-70 m). The bottom phase of dives by guillemots was relatively long, indicating that they spent considerable time searching for and pursuing prey. Guillemots also spent a greater proportion of each dive bout underwater and had faster rates of descent, indicating that they were more adept at maximising time for pursuit and capture of prey. These differences in foraging behaviour may partly reflect guillemots feeding their chicks single large prey obtained near the bottom and razorbills feeding their chicks multiple prey from the water column. Nonetheless, our data support the notion that interspecific differences in wing loadings of auks reflect an evolutionary trade-off between aerial and underwater locomotion.

Fine-scale foraging behaviour of a medium-ranging marine predator.

1. Movement patterns of predators should allow them to detect and respond to prey patches at different spatial scales, particularly through the adoption of area-restricted search (ARS) behaviour. Here we use fine-scale movement and activity data combined with first-passage time (FPT) analysis to examine the foraging strategy of northern gannets Morus bassanus in the western North Sea, and to test the following hypotheses: (i) birds adopt a hierarchical foraging strategy characterized by nested ARS behaviour; (ii) the locations and characteristics of ARS zones are strongly influenced by physical oceanography; (iii) the initiation of ARS behaviour is triggered by the detection and pursuit of prey; (iv) ARS behaviour is strongly linked to increased foraging effort, particularly within nested ARS areas. 2. Birds on 13 of 15 foraging trips adopted ARS behaviour at a scale of 9.1 +/- 1.9 km, and birds on 10 of these 13 trips adopted a second, nested ARS scale of 1.5 +/- 0.8 km, supporting hypothesis 1 above. ARS zones were located 117 +/- 55 km from the colony and over half were within 5 km of a tidal mixing front ~50 km offshore, supporting hypothesis 2 above. 3. The initiation of ARS behaviour was usually followed after only a short time interval (typically ~5 min) by the commencement of diving. Gannets do not dive until after they have located prey, and so this pattern strongly suggests that ARS behaviour was triggered by prey detection, supporting hypothesis 3 above. However, ~33% of dives in mixed coastal water and 16% of dives in stratified water were not associated with any detectable ARS behaviour. Hence, while ARS behaviour resulted from the detection and pursuit of prey, encounters with prey species did not inevitably induce ARS behaviour. 4. Following the initiation of ARS behaviour, dive rates were almost four times higher within ARS zones than elsewhere and almost three times higher in zones with nested ARS behaviour than in those without, supporting hypothesis 4 above and suggesting that the foraging success of birds was linked to their ability to match the hierarchical distribution of prey.

Parasite treatment affects maternal investment in sons.

Parasitism can be a major constraint on host condition and an important selective force. Theoretical and empirical evidence shows that maternal condition affects relative investment in sons and daughters; however, the effect of parasitism on sex ratio in vertebrates is seldom considered. We demonstrate experimentally that parasitism constrains the ability of mothers to rear sons in a long-lived seabird, the European shag Phalacrocorax aristotelis. The effect contributes to the decline in offspring survival as the breeding season progresses and hence has important population-level consequences for this, and potentially other, seasonal breeders.

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.

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.

Tick-borne Great Island Virus: (II) Impact of age-related acquired immunity on transmission in a natural seabird host.

Tick-borne pathogen transmission is dependent upon tick number per host and the physical and temporal distribution of each feeding stage. Age-related acquired immunity to tick and pathogen may also be important but has received less attention. In this study we evaluate which of these parameters has the greatest impact on Great Island Virus (GIV) transmission between Ixodes uriae ticks and common guillemots (Uria aalge). The study system is well suited to investigate age-related effects because the guillemot population is naturally divided into 2 groups, older breeding and younger pre-breeding adult birds. The physical distribution and timing of adult and nymphal tick feeding was similar for both guillemot age groups. However, breeding birds were parasitized by significantly more ticks (mainly nymphs). Calculations based on tick number predict virus prevalence should be higher in ticks that have fed on breeding rather than pre-breeding birds. However, empirical evidence indicates the reverse. Protective acquired immunity to GIV infection may be the reason why GIV prevalence is actually significantly lower in ticks that have fed on breeders. Far more breeding (74%) than pre-breeding (12%) guillemots had antibodies that neutralized 1 or more GIV strains. Estimates of the force of infection support the view that pre-breeding birds experience higher rates of virus infection than breeding birds. The results indicate age-related acquired immunity is a key factor in GIV transmission and highlight the need to consider age-related effects and host immunity when undertaking quantitative studies of tick-borne pathogen transmission.

Tick-borne Great Island Virus: (I) Identification of seabird host and evidence for co-feeding and viraemic transmission.

Great Island Virus (GIV) is an arbovirus present in the tick Ixodes uriae, a common ectoparasite of nesting seabirds. Common guillemot (Uria aalge) and black-legged kittiwake (Rissa tridactyla) are the preferred and most abundant hosts of I. uriae on the Isle of May, Scotland. As part of a study to understand the epidemiology of GIV, the ability of guillemot and kittiwake to support tick-borne transmission of GIV was examined. GIV was present in ticks feeding in isolated guillemot colonies and guillemots had virus-specific neutralizing antibodies demonstrating previous GIV infection. By contrast, only uninfected ticks were found in colonies inhabited solely by kittiwakes. GIV was isolated from kittiwake ticks in colonies which also contained breeding guillemots but no virus-specific neutralizing antibodies were present in blood samples of kittiwake on which infected ticks were feeding. Thus guillemots are the main vertebrate hosts of GIV on the Isle of May whereas kittiwakes do not appear to be susceptible to infection. Virus infection of adult ticks feeding on guillemots was highly efficient and may involve both viraemic transmission and transmission from infected to uninfected ticks feeding together on birds that do not develop a patent viraemia.

Modelling the spatial distribution of ammonia emissions from seabirds in the UK.

Knowledge of the sources and distribution of ammonia (NH3) emissions underpins our understanding of the nitrogen budget. Research has focused on quantifying NH3 emissions from anthropogenic sources, whilst those from natural sources have received little attention internationally. Seabirds excrete large quantities of nitrogen, making seabird colonies a major natural source of NH3. Ammonia emissions from each UK seabird species were estimated and combined with population distribution data to model their spatial distribution. Total NH3 emissions from UK seabirds were estimated at 2.7 kt per year. Seabird emissions are concentrated in remote parts of the UK where anthropogenic emissions are small, so that seabirds often represent the main source of NH3 emissions in these areas. Seabird NH3 emissions were found to have increased by 34% since the 1970s. This corresponds to population changes which may be influenced by human activities, showing that even this natural source can be anthropogenically modified.

Sex-specific foraging behaviour in a monomorphic seabird.

Sexual differences in the foraging behaviour of parents have been observed in a number of sexually sizedimorphic birds, particularly seabirds, and the usual inference has been that these sex-specific differences are mediated primarily by differences in body size. To test this explanation, we compared the foraging behaviour of parents in a monomorphic seabird species, the northern gannet Morus bassanus. Using specially designed instruments and radio telemetry we found that individuals of both sexes were consistent in the directions and durations of their foraging trips. However, there were significant differences in the foraging behaviour of males and females. Female gannets were not only more selective than males in the areas where they foraged, but they also made longer, deeper dives and spent more time on the sea surface than males. As the sexes are morphologically similar in this species, then these differences are unlikely to have been mediated by body size. Our work highlights the need to investigate sexual differences in the foraging behaviour of seabirds and other species more closely, in order to test alternative theories that do not rely on differences in body size.

Evidence of intra-specific competition for food in a pelagic seabird.

The factors affecting the population dynamics of seabirds have long intrigued biologists. Current data suggest that density-dependent depletion of prey during the breeding season may regulate population size. However, much of the evidence for this has been circumstantial, and the underlying mechanisms are unclear. Here, we show that the per capita population growth rates of northern gannet Morus bassanus at colonies in Britain and Ireland have declined with increasing population size. Furthermore, direct observations reveal that the mean foraging trip duration of breeding gannets is positively correlated with colony size, both among colonies of different sizes in the same year, and within colonies as they change in size. To understand this phenomenon, we have developed a model which demonstrates that disturbance of fish alone can readily generate conditions under which gannets at larger colonies have to travel further to obtain food.

The activity periods and life-cycle of the tick Ixodes uriae (Acari: Ixodidae) in relation to host breeding strategies.

We investigated the timing of seasonal activity of the seabird tick Ixodes uriae by examining engorgement rates of off-host ticks and the prevalence of infested common guillemots (Uria aalge) and kittiwakes (Rissa tridactyla) on the Isle of May, Scotland. More than 99% of I. uriae fed during the period late April to early August which coincided with the seabird breeding season. No ticks fed in the autumn and winter, and none over-wintered in the engorged state. Peak tick feeding activity was during the hosts' incubation period in May and early June, when over 70% of birds were parasitized. Few ticks were active when guillemot chicks were being brooded, or during the early part of kittiwake chick-rearing. Adult female tick feeding peaked in the first week of June, while nymphal and larval activity peaked in the third week of May. Adult female ticks fed later than nymphs on guillemots and larvae on both guillemots and kittiwakes; however, there was considerable temporal overlap in the feeding periods of the 3 stages of both hosts. All larvae and nymphs fed in May and early June, but up to 18% of adult females remained unengorged at this time, and probably deferred feeding by 1 year. A small proportion of individuals which fed as larvae in May appeared to feed again as nymphs in July of the same season, thereby shortening their life-cycle by 1 year. The duration of the life-cycle of I. uriae on the Isle of May is typically 3 years but varies from 2 to 4 years. Ticks feeding on guillemots did so significantly earlier than those feeding on kittiwakes, possibly because guillemots start breeding earlier in the year. Breeding of both guillemots and kittiwakes was later in 1994 than in 1993. This delayed the activity of all tick stages on kittiwakes and adult female ticks on guillemots, but did not affect the timing of activity of nymphs or larvae feeding on guillemots.