Temporal Changes in Tick-Borne Pathogen Prevalence in Questing Ixodes ricinus Across Different Habitats in the North-Eastern Italian Alps

Changes in land use, climate, and host community are leading to increased complexity in eco-epidemiological relationships and the emergence of zoonoses. This study investigates the changes in the prevalence of several Ixodes ricinus-transmitted pathogens in questing ticks over a 10-year interval (2011–2013, 2020) in natural and agricultural habitats of the Autonomous Province of Trento (North-eastern Alps), finding an average prevalence of infection of 27.1%. Analysis of 2652 ticks, investigating four infectious agents (Borrelia burgdorferi sensu lato, Anaplasma spp., Rickettsia spp., and Babesia spp.), revealed the circulation of 11 different zoonotic pathogens, with varying infection rates across different years and habitats. In 2020, we found a decrease in Anaplasma phagocytophilum, associated with agricultural habitats, and Rickettsia spp., found in all habitats. In the same year, Babesia spp. increased in both habitats, similar to Borrelia burgdorferi sensu stricto, which was related to natural habitats. Co-infections were identified in 8% of positive-tested ticks with different spatiotemporal associations, primarily in natural settings. Our results provide new evidence that the risk of infection with tick-borne pathogens in the Alpine region varies over time and in different environments, broadening the current information on co-infection rates and the circulation of zoonotic pathogens, previously not reported in this area.