Ecological Factors Characterizing the Prevalence of Bacterial Tick-Borne Pathogens in Ixodes ricinus Ticks in Pastures and Woodlands

Abstract

Ecological changes are recognized as an important driver behind the emergence of infectious diseases. The prevalence of infection in ticks depends upon ecological factors that are rarely taken into account simultaneously. Our objective was to investigate the influences of forest fragmentation, vegetation, adult tick hosts, and habitat on the infection prevalence of three tick-borne bacteria, Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, and Rickettsia sp. of the spotted fever group, in questing Ixodes ricinus ticks, taking into account tick characteristics. Samples of questing nymphs and adults were taken from 61 pastures and neighboring woodlands in central France. The ticks were tested by PCR of pools of nymphs and individual adults. The individual infection prevalence was modeled using multivariate regression. The highest infection prevalences were found in adult females collected in woodland sites for B. burgdorferi sensu lato and A. phagocytophilum (16.1% and 10.7%, respectively) and in pasture sites for Rickettsia sp. (8.7%). The infection prevalence in nymphs was lower than 6%. B. burgdorferi sensu lato was more prevalent in woodlands than in pastures. Forest fragmentation favored B. burgdorferi sensu lato and A. phagocytophilum prevalence in woodlands, and in pastures, the B. burgdorferi sensu lato prevalence was favored by shrubby vegetation. Both results are probably because large amounts of edges or shrubs increase the abundance of small vertebrates as reservoir hosts. The Rickettsia sp. prevalence was maximal on pasture with medium forest fragmentation. Female ticks were more infected by B. burgdorferi sensu lato than males and nymphs in woodland sites, which suggests an interaction between the ticks and the bacteria. This study confirms the complexity of the tick-borne pathogen ecology. The findings support the importance of small vertebrates as reservoir hosts and make a case for further studies in Europe on the link between the composition of the reservoir host community and the infection prevalence in ticks.

Longitudinal field study on bovine Babesia spp. and Anaplasma phagocytophilum infections during a grazing season in Belgium

“…EU1, it would raise implications for the epidemiology and control of this zoonotic parasite. Wild cervids appear to act as a reservoir host for A. phagocytophilum (Rosef et al 2009) as do probably cattle (de la Fuente et al 2005b;Halos et al 2010).…”

“…EU1 has been recorded recently in Belgium (Lempereur et al 2011). Anaplasma phagocytophilum is a polymorphic gramnegative bacterium that strictly parasitizes mammals; wild and domestic animals are the main reservoirs (Halos et al 2010), but infection is potentially zoonotic causing human granulocytic anaplasmosis (HGA). The symptoms of this disease vary from asymptomatic infection to severe disease by way of nonspecific flu-like clinical signs (Bakken and Dumler 2008;Thomas et al 2009).…”

Pathogen-mediated manipulation of arthropod microbiota to promote infection

“…scapularis model, distinct differences were noted in the relative abundance and composition of the microbiota of ticks feeding on uninfected, or A. phagocytophilum-infected, mice, indicating that the presence of A. phagocytophilum alters the tick gut microbial community. Numerous factors including exposure to environmental bacteria, geographic location, tick species, gender, developmental status, and time since molting and feeding, among others, are expected to play an important role in contributing to the microbiome composition in ticks (10,44,45). Therefore, although the tick gutassociated microbes might not be conserved across different regions, with several published reports suggesting a large diversity (46)(47)(48)(49), and others suggesting that inflated diversities are due to environmental contaminants (50), we used multiple criteria (see SI Appendix) to accurately assess the microbial composition of our laboratory-reared and murine host-fed I. scapularis nymphs.…”

Experimental evidence that livestock grazing intensity affects cyclic vole population regulation processes

“…For example, there's no empirical evidence supporting a relationship between ungulate grazing and trans-generational effects in voles. Indirect effects of grazing on landscape structure and connectivity might influence macro-parasite prevalence and transmission (Brownstein et al 2005;Halos et al 2010), so that grazing intensity and vole parasitism might be linked. Grazing impact on landscape structure and connectivity might also have influenced predator foraging opportunities, e.g., by increasing avian predation or decreasing risk-averse mustelid foraging behaviour (Zub et al 2008), conceivably leading to a net reduction in delayed density dependence (Bjørnstad et al 1995;Hanski et al 2001).…”