Anthelmintic treatment and the stability of parasite distribution in ruminants

Simple Summary: Parasites tend to be unevenly distributed among hosts, with most hosts in a population carrying few parasites and most of the parasites found in a few heavily infected individuals. This property, known as aggregation or overdispersion, is important to the diagnosis of parasite infections in groups of animals and their management. Analysis of 325 sets of gastrointestinal nematode parasite counts from wild and domestic ruminants, some including worms from post-mortem examinations and others faecal egg counts, explored how overdispersion changed in relation to various factors. A systematic relationship was found between the variance in parasite counts and their means, in accordance with the previously demonstrated Taylor’s power law. Furthermore, groups of livestock frequently treated with anthelmintics had more aggregated parasite burdens. For parasite species that stimulate strong immunity, aggregation was lower for faecal egg counts than for adult worm burdens. Considered together, the results suggest that immunity to parasites tends to stabilise distributions and that treatment interferes with this process and leads to greater clustering of infections among individuals. Understanding the processes that drive parasite aggregation will help to manage them in farmed systems and more generally could shed light on how animal distributions are shaped in changing environments. Abstract: Parasites are generally overdispersed among their hosts, with far-reaching implications for their population dynamics and control. The factors determining parasite overdispersion have long been debated. In particular, stochastic parasite acquisition and individual host variation in density-dependent regulation through acquired host immunity have been identified as key factors, but their relative roles and possible interactions have seen little empirical exploration in parasite populations. Here, Taylor’s power law is applied to test the hypothesis that periodic parasite removal destabilises the host-parasite relationship and increases variance in parasite burden around the mean. The slope of the power relationship was compared by analysis of covariance among 325 nematode populations in wild and domestic ruminants, exploiting that domestic ruminants are often routinely treated against parasite infections. In Haemonchus spp. and Trichostrongylus axei in domestic livestock, the slope increased with the frequency of anthelmintic treatment, supporting this hypothesis. In Nematodirus spp., against which acquired immunity is known to be strong, the slope was significantly greater in post-mortem worm burden data than in faecal egg counts, while this relationship did not hold for the less immunogenic genus Marshallagia. Considered together, these findings suggest that immunity acting through an exposure-dependent reduction in parasite fecundity stabilises variance in faecal egg counts, reducing overdispersion, and that periodic anthelmintic treatment interferes with this process and increases overdispersion. The results have implications for the diagnosis and control of parasitic infections in domestic animals, which are complicated by overdispersion, and for our understanding of parasite distribution in free-living wildlife. Parasite-host systems, in which treatment and immunity effectively mimic metapopulation processes of patch extinction and density dependence, could also yield general insights into the spatio-temporal stability of animal distributions.