Sand lizards (Lacerta agilis) decrease nymphal infection prevalence for tick-borne pathogens Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in a coastal dune ecosystem

Abstract

Understanding which factors determine tick-borne disease hazard can contribute to effective disease control. In Europe, the hazard of the pathogens Borrelia burgdorferi s.l. and Anaplasma phagocytophilum is determined by local tick densities (mainly Ixodes ricinus) and the reservoir competence of the host species community. Sand lizards (Lacerta agilis) are common hosts for larvae and nymphs of I. ricinus and non-competent reservoirs for both pathogens. Consequently, high relative abundance of L. agilis is hypothesized to be associated with lower infection prevalence in nymphs. Here, we aimed to test whether this effectively occurs in natural settings. We sampled different habitat types within a heterogenous dune landscape at the Dutch coast and estimated (1) L. agilis densities, (2) host community competence, (3) the density and infection prevalence of questing I. ricinus ticks and (4) the number and infection prevalence of ticks feeding on L. agilis. Captured L. agilis had high tick burdens and contributed substantially to feeding I. ricinus larvae in their natural habitat. B. burgdorferi s.l. and A. phagocytophilum were virtually absent from feeding larvae and nymphs. The nymphal infection prevalence of both pathogens in questing ticks was lower in habitat types where L. agilis was more abundant. Hence, L. agilis strongly reduced community competence. The density of questing nymphs was higher in habitat types with denser vegetation and also varied more between habitat types than infection prevalence. As a result, nymphal density had a stronger effect on the density of infected ticks than did nymphal infection prevalence. Synthesis and applications. Coastal dune habitats favourable for L. agilis have lower densities of questing nymphs and a lower human infection hazard. These results might be applicable to similar ecosystems where L. agilis is present. From a public health perspective, this underlines the importance of preserving early successional habitat, as encroaching shrubs are associated with higher tick-borne disease hazard, and vegetation removal might be a solution to reduce hazard in coastal dunes. The high degree of spatial heterogeneity in the abundance of tick-borne pathogens also poses opportunities to manage recreational activities to limit human exposure to tick-borne diseases.