Tick-borne diseases are a growing public health concern globally as their incidence is rising. However, the spatiotemporal dynamics of questing ticks infected with human pathogens such as the Lyme borreliosis bacteria, remain largely unclear. We investigated the transmission dynamics of common tick-borne pathogens, focusing mainly on Borrelia burgdorferi sensu lato (‘Borrelia’) and the impact of ecological interactions between ticks, hosts and forest types on Lyme borreliosis risk. Forest composition and structure have been shown to affect the density of ticks, but their impact on the prevalence of Borrelia in the ticks has not been investigated so far. The study of the impact of forest type on Lyme borreliosis risk is particularly important in the context of the ongoing conversion of homogeneous coniferous forests to more natural, mixed forests dominated by indigenous broadleaved trees in many regions in Europe.
According to the dilution effect hypothesis, postulated in North America, a forest with a high diversity of hosts for ticks contains more hosts that are poorly capable of transmitting Borrelia to ticks compared to a forest with a species-poor host community, consisting mostly of transmission-competent host species. This hypothesis has not yet been tested in Europe, where different types of hosts transmit different Borrelia genospecies.
In the Kempen, northern Belgium, we studied forest stands of four forest types: oak or pine stands, with or without a substantial shrub layer. These forest types are representative for the different stages in the process of forest conversion. In this part of the study, we focused on Borrelia afzelii, the most common Borrelia genospecies in Lyme borreliosis patients in Western Europe and transmitted to ticks by small rodents. We found that the density of Ixodes ricinus ticks or the infection prevalence of Borrelia in ticks from our study sites did not increase from 2009 to 2014, similar to the reported stable incidence of Lyme borreliosis and tick bites in Belgium. The density of ticks, rather than the infection prevalence of B. afzelii, was more important in explaining variation in the density of infected ticks and can thus be used as a predictor of disease risk. The density of ticks was higher in oak stands than in pine stands, but the prevalence of B. afzelii was highest in pine stands. We could not confirm the dilution effect hypothesis; the density of infected ticks, a commonly used risk measure in the literature, was not correlated with host diversity, and the host diversity did not differ between the forest types. Our results indicate differential host use by ticks in different habitats, with larvae feeding more often on small rodents in pine stands and more on other types of hosts, such as birds, which transmit genospecies other than B. afzelii, in oak stands.
Besides in forests, the favourable habitat of I. ricinus, humans are also exposed to ticks and human pathogens in (sub)urban green spaces. We found many common human pathogens, such as Borrelia genospecies, Borrelia miyamotoi and Anaplasma phagocytophilum, in squirrels and ticks from hedgehogs collected in urban settings. Hence, humans are likely to encounter ticks infected with one or several pathogens while gardening or recreating in parks.
We conclude that focusing on the dilution effect to reduce Lyme borreliosis risk is not an effective management option in our study region, and possibly in other European regions with similar forest communities. Instead of decreasing Lyme borreliosis risk, adding host species to the host community can even increase disease risk, by increasing the prevalence of Borrelia genospecies that give rise to clinical manifestations of Lyme borreliosis such as neuroborreliosis that are more severe compared to skin manifestations (mainly caused by B. afzelii). Lyme borreliosis prevention should therefore aim to reduce tick densities and the contact rate between ticks and humans. The risk for human exposure to Lyme borreliosis not only depends on the density of infected ticks but importantly also on the human-tick contact rate. Our results suggest that decreasing the density of (infected) ticks will rarely lead to a substantially lower Lyme borreliosis risk. Forest management can decrease the human-tick contact rate and the subsequent Lyme borreliosis risk by directing visitor flows, e.g. along points of attraction or marked-out routes, and by mowing the vegetation along trails.