Early signals of parasitism expressed through changes in host activity and social behaviour

Abstract

Parasites are ubiquitous in the environment and can profoundly impact the health and welfare of their hosts. Infected animals will often exhibit an array of behavioural responses that are termed sickness behaviours. By exhibiting these behaviours, animals can potentially reallocate energetic resources to reduce the severity of infection. However, focusing energetic resources to fight infection could remove resources from other activities that are more beneficial to host fitness. Infected animals may therefore, modulate their behavioural response to infection across different environments including their social environment.

This thesis comprises a series of experimental work in a domestic sheep (Ovis aries) system. I first validated two remote monitoring systems (activity monitors and proximity loggers) (Chapter 2) that would be used to record the activity and social behaviour of lambs. The validation work aimed to compare the level of agreement between the behaviours recorded using remote monitoring systems and live focal observations during a series of experiments and evaluate the capabilities of the proximity system to be used in future hypothesis testing. In Chapter 2, I found a positive correlation between live behavioural observations and the data collected by the remote sensors. However, proximity loggers provided a more detailed representation of animal behaviour and could detect subtle changes in behaviour earlier than what could be detected using focal observations.

I then carried out a large-scale field trial to investigate how parasite infection affects the activity behaviour (Chapter 3) and social behaviour (Chapter 4) of groups of lambs of different parasitic status, to understand what stages of infection these behavioural changes occur, and what affect the infection status an individual’s social group can have on their behavioural response to infection. I monitored the activity and social contact behaviour of lambs during four phases of infection (pre-parasite, pre-patent; patent-parasite, post-parasite). Lambs were part of one of three treatments: Parasitised; all lambs were experimentally infected with the gastrointestinal nematode Teladorsagia circumcincta, Non-parasitised; all lambs were given a sham infection and dosed with water, Mixed; part of the group were infected with T. circumcincta, and part of the group were dosed with water. Faecal samples were taken each week to measure the number of nematode eggs per gram of faeces, blood samples were taken at three time points to measure serum pepsinogen levels to give an indication of gut wall damage and lambs were weighed weekly to measure liveweight gain. Analysis of the animals’ measurements (faecal egg counts, pepsinogen levels and weight) demonstrated experimental infection was successful in all cases and lambs to remain parasite free remained clear of parasites throughout the study (Chapter 3 and 4).

In Chapter 3, I found that parasitism affects the activity behaviour of lambs in both single-parasitic state and mixed-parasitic state groups immediately after exposure to parasitism, during the pre-patent phase, three weeks before parasitism could be detected through standardised assessment measures of parasitism and before any noticeable impact of parasitism on physiological measures or condition/weight. However, the extent of this behaviour change was affected by the infection status of an individual’s social group. I also show that following treatment with anthelmintic, the behaviour of infected animal’s returns to pre-parasite levels, providing further evidence these effects are a direct consequence of parasitism.

In Chapter 4, I found that all individuals in the parasitised groups had reduced contact frequency during the pre-patent, patent-parasite and post-parasite phases, but increased duration of contacts during the pre-patent phase. There was also a reduction in the frequency of contacts in the mixed groups relative to the non-parasitised groups; however this was driven by a reduction in contacts between infected individuals only, as there was no change in the social contact behaviour between infected and non-infected animals. I also found that although infected animals in mixed-state groups had reduced contact frequency, there was no change in the network architecture of the group as non-infected animals maintained pre-infection levels of social interactions.

These results show that parasitism can affect the activity and social behaviour of infected individuals. However, in mixed-parasitic state groups the parasitic status of other group members can socially modulate the behaviour of both infected and non-infected individuals. Moreover, given the social effects of parasitism and the impact on traits associated with host fitness as well as on behaviour, this research highlights that parasite-mediated behavioural changes can vary due to an individual’s social environment. This may have implications for our understanding of how sociality impacts infection across different populations.