Assessing zoonotic risk in a fenced natural park in northwestern Italy: integrating camera traps for a vector-host approach to investigate tick-borne pathogens

Abstract

Tick-borne diseases are among the major widespread emerging zoonotic diseases, and their circulation in the environment is influenced by a broad range of abiotic and biotic factors, including the abundance of vectors and vertebrate hosts. In this study, we estimated the prevalence of tick-borne pathogens and the impact of wildlife head count on their circulation in a lowland natural area in northwestern Italy. We collected ticks and camera trap pictures from 14 sampling points every 2 weeks for 1 year and identified pathogens through molecular analyses: Babesia capreoli, B. microti-like, Borrelia burgdorferi sensu lato (s.l.), Rickettsia of the spotted fever group (SFG), Theileria capreoli, and Anaplasma phagocytophilum. We modeled the presence of B. capreoli, B. microti-like, B. burgdorferi s.l., and SFG Rickettsia on head counts of wild ungulates and mesocarnivores. We tested a global model including all collected ticks, as well as a model focusing solely on Ixodes ricinus nymphs, the species, and the developmental stage most associated with zoonotic infection risk. The highest prevalence was obtained for B. microti-like (13%) and SFG Rickettsia (11%), and, for most pathogens, no differences were detected among tick species and their developmental stages. Mesocarnivores showed an additive effect on B. microti-like and B. burgdorferi s.l., while wild ungulates, non-competent for transmission of our target pathogens, showed a dilutive effect. These findings confirm the circulation of relevant tick-borne pathogens in the study area and show the use of camera trap data in predicting tick-borne pathogens' risk by targeting host species which may have an indirect impact and are more easily addressed by monitoring and control strategies.

Keywords: Ixodidae; humans; recreational areas; tick-borne zoonoses; wildlife.

Figure 1

Location of La Mandria Natural Park in the Piedmont region (Italy), with reference to the regional capital, Turin.

Figure 2

Pathogen positivity across the months per developmental stage. For each of the targeted pathogens, the percentage of positive pools over the total number of collected pools in each month is shown on the primary y-axis. Winter months (December, January, and February) were excluded due to a lack of tick activity. The blue line (secondary y-axis) represents ticks’ abundance (log-scaled average of number of ticks collected in each sampling point). (A) Represents the total number of ticks. (B) Represents the number of larvae. (C) Represents the number of nymphs. (D) Represents the number of adults.

Figure 3

Model result coefficients. Coefficients (blue, positive; red, negative) of the models for each pathogen in the global model (A–D) and in the I. ricinus nymph model (E–H). Asterisks indicate statistical significance. Silhouettes on the x-axis represent mesocarnivores head count (fox), total number of ticks in the pool (tick), wild ruminants head count (red deer), and wild boar head count (wild boar).