Individual variation in chronic and acute parasitism in seabirds

Abstract

Parasitism is ubiquitous in wild populations, with host-parasite interactions forming an integral aspect of ecosystems. Infections with parasites can range from acute to chronic, and lead to sublethal or lethal impacts on hosts. Individual hosts may vary in their exposure, susceptibility, tolerance to parasitism, which can be linked to both intrinsic differences between individuals and extrinsic factors which may vary in both space and time. Seasonal variation in host life histories, such as the timing of breeding, conditions during early life or variation in migratory strategies can vary between components of the host population. This variation may lead to different experiences of extrinsic factors such as resources, exposure to parasites or environmental conditions, culminating in variation in the prevalence and abundance of infection, and its fitness consequences. Investigating the links between individual variation and parasitism is crucial to understanding the impacts of disease on wild populations. As anthropogenic driven environmental change alters host life history patterns, and increases the rate of infectious disease emergence with impacts across species boundaries, such understanding is vital for predicting and mitigating against the impacts of parasitism on wildlife, domestic animal and human health.

In this thesis we investigate how variation in host traits and life history is associated with chronic and acute infections, with a focus on seasonal variation. We focus on an individually marked population of colonially breeding, partially migratory wild seabirds, European shags (Gulosus aristotelis), on the Isle of May in Scotland, a population where life history data is collected throughout life. This population shows extensive variation seasonal life history, both in the timing of breeding, leading to seasonal differences in early life of offspring, and in migration, with some individuals migrating and others remaining resident during the non-breeding season. We investigate the responses to two types of parasites on shag hosts: chronic infections caused by nematode gut parasites and acute infections caused by avian paramyxovirus-1, the causative agent of Newcastle disease.

Firstly, we use 8 years of data on individual nematode parasite burdens to investigate how temporal variation in early life (during the natal year) and breeding conditions impact infection throughout life. We reveal sex differences in the impact of current and early-life conditions on nematode burdens. In breeding adults, female burdens vary according to seasonality in current conditions but early life effects are more important in males. We found seasonal variation in burdens associated with current conditions: later breeding adult females and later hatched young of both sexes had higher burdens than birds from earlier breeding events. For males, we found that those that had hatched later in the season when they were chicks (early life conditions) had lower burdens when they were adults. Second, we therefore considered the importance of early life parasitism and hatching phenology, using a parasite manipulation experiment to investigate trade-offs between parasitism, growth and immunity across the nestling period in chicks. We find that hatch date was associated with differences in immune cell counts, but that these relationships were not mediated by parasitism. Third, we move on from chronic macro-parasite infections to compare the importance of seasonal behaviour and sex in shaping exposure and susceptibility to an acute microparasite infection, for which cormorant species are known to be a reservoir. We use multiple years of antibody data to investigate patterns of avian paramyxovirus-1, in shag chicks and adults. We found evidence of consistent but fluctuating prevalence of antibodies across years in adults, which produced differences in antibody profiles of their offspring, with maternal antibodies detected in recently hatched chicks of positive females. In adults, antibody prevalence was higher in females than males, but did not differ between migrants and residents. Finally, in response to an unprecedented outbreak of another viral pathogen in seabirds, highly pathogenic avian influenza, we develop a minimally invasive, and logistically beneficial method for the detection of viral antibodies in multiple species of seabird. We find it is possible to differentiate antibody positive and negative individuals using cloacal and choanal swabs, but the sensitivity of the technique is low and variable between swab type and species. Further feedback between field collection and laboratory optimisation is required before this technique can provide a useful tool for wildlife disease surveillance.

The findings of this thesis highlight that individual variation in host traits shape host burden and responses to infection across both acute and chronic infections in wild populations. By monitoring individuals across their life time, we find that sex differences, seasonality and early life conditions are key in mediating the relationship of individual hosts with both chronic and acute parasitism. These studies emphasise the importance of long-term population studies for understanding individual level responses to parasitism.