The roles of contrasting host types on the environmental abundance of Anaplasma phagocytophilum, an emerging zoonotic pathogen

William McLellan , Sara Gandy, Lucy Gilbert, Mara Rocchi, Fanny Olsthoorn, Jaboury Ghazoul, Jude Eze, Livia May, Hein Sprong

Fundamental knowledge of the role of hosts in shaping vector-borne pathogen abundance is critical to understanding the ecology of these disease systems; yet the roles can be challenging to tease apart, especially for pathogens vectored by generalist feeders with multiple hosts. In this study, we aimed to quantify the relative contributions of hypothesised pathogen transmission hosts (deer and sheep) and non-transmission hosts (birds and rodents) to the environmental abundance of Anaplasma phagocytophilum (ecotypes I and II) in Ixodes ricinus ticks. Anaplasma phagocytophilum is a zoonotic pathogen, vectored by I. ricinus, that causes tick-borne fever in livestock and anaplasmosis in humans. We collected data on A. phagocytophilum prevalence and environmental hazard (density of infected ticks at 40 sites), sheep presence (at 40 sites) and relative abundance indices of deer (at 40 sites) rodents (at 20 sites) and birds (at 10 sites) in northwest Scotland between 2018 and 2020. As predicted, deer were positively associated with A. phagocytophilum prevalence and hazard, indicating their potential role as pathogen transmission hosts. In contrast, bird abundance was negatively associated with A. phagocytophilum prevalence, indicating that higher bird densities may divert more ticks away from feeding on transmission hosts, thus reducing A. phagocytophilum prevalence. This highlights the importance of including non-transmission hosts when examining environmental disease risk factors. Sheep presence and rodent abundance index did not significantly influence A. phagocytophilum prevalence and hazard at our sites. Our findings could have implications for conservation and disease mitigation as land management practices that reduce deer density and promote bird abundance could reduce A. phagocytophilum prevalence and hazard.