Hanna Granroth-Wilding

PhD thesis

Parasitism, Family Conflict and Breeding Success
University of Edinburgh
2013

Download the thesis (PDF)

Supervisors: Emma Cunningham and Sue Lewis at Edinburgh University, Francis Daunt and Sarah Burthe at the Centre for Ecology & Hydrology.

Lay summary

Wild animals are almost always infected with large numbers of parasites. A parasite infection can be expensive for the host to deal with, leading to negative consequences such as less successful breeding or poorer survival. By altering these vital rates, effects of parasites on individual hosts have the potential to scale up and affect the dynamics of entire populations. However, different hosts suffer these effects to different extents. Intrinsically, some may be more able to cope with an infection, for example because they are in better condition or have more efficient immune systems. Hosts may also be subject to different extrinsic influences, including both their ecological environment, for example food availability, and their social environment, that is how they interact with other individuals. These differences between hosts could be especially important during breeding, when parents must weigh up how much to invest in their own parasite defences against investing in caring for their young, who may be particularly vulnerable to infection. In this thesis, I investigate how parasite infection of nestling chicks and their parents influences these trade-offs between family members and how this affects the outcome of the breeding attempt. I use experimental anti-parasite treatment of the European shag Phalacrocorax aristotelis to examine the role of gut parasites in chick growth and survival, behavioural interactions between chicks and their parents, parent condition and parents' behaviour during and after the breeding season. As a seabird, the shag is an important indicator of changes in the marine environment, and understanding its responses to these changes requires a full understanding of its ecology. Parasitism is an important part of this ecology that has until recently been overlooked.

Full abstract

Parasites are important drivers of ecological and evolutionary processes in their hosts. However, hosts often differ in how they are affected by parasitism, which can be important in how parasite effects on individuals scale up to the population level. Hosts may differ intrinsically in their susceptibility to parasitism, and extrinsic factors may impose constraints on how hosts allocate resources between immunity, maintenance and reproduction, thereby further affecting their ability to cope with infection. These extrinsic factors include the host's ecological environment, for example food availability or weather, and its social environment, that is its interactions with conspecifics. This is particularly true during a reproductive attempt when individuals interact closely with other family members. Not only might immediate impacts of parasitism differ between and within parents and offspring, but the direct effects of parasitism on a host could have further indirect consequences for other family members through their behavioural interactions with parasitised individuals. The distribution of direct and indirect effects among all family members could affect the outcome of the breeding event and individuals' future performance. However, teasing apart these various avenues of parasite impacts on families may be difficult if parasite burden or susceptibility is correlated between family members. In this thesis, I explore the consequences of parasitism for different family members of the European shag Phalacrocorax aristotelis infected with gastrointestinal nematodes, over a range of ecological conditions.

In chapter 2, I demonstrate that chicks' responses to anti-parasite treatment across four years vary between siblings and with environmental conditions, which may be mediated by resource allocation among siblings. In chapter 3, I explore how costs of parasitism are distributed among the whole family by simultaneously treating chicks and/or parents with an anti-parasite drug and measuring the outcomes for all family members. Treatment has a more marked effect for the non-treated generation than for the treated individuals, suggesting that parasitism may have important indirect costs. In chapter 4, I investigate whether within-brood variability in the effects of anti-parasite treatment and its cross-generational impacts are mediated by behavioural change, and show that chick treatment but not parent treatment influences several aspects of behaviour in the nest. In chapter 5, I demonstrate that the impact of chick anti-parasite treatment on parents persists beyond the breeding attempt, with parents of treated chicks foraging less overwinter and breeding earlier the following year, whereas there is no persistent effect of parents' own anti-parasite treatment. Lastly, I provide an appendix examining the parasitology of the system in detail, including an assessment of in situ and proxy measures of worm burdens of chicks. This thesis demonstrates that parasitism can be a key component, previously overlooked, of reproductive performance in seabirds, a group that plays an important ecological role as apex predators and thus indicator species of the marine environment.