Effect of Climate and Land Use on the Spatio-Temporal Variability of Tick-Borne Bacteria in Europe

Abstract

The incidence of tick-borne diseases caused by Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Rickettsia spp. has been rising in Europe in recent decades. Early pre-assessment of acarological hazard still represents a complex challenge. The aim of this study was to model Ixodes ricinus questing nymph density and its infection rate with B. burgdorferi s.l., A. phagocytophilum and Rickettsia spp. in five European countries (Italy, Germany, Czech Republic, Slovakia, Hungary) in various land cover types differing in use and anthropisation (agricultural, urban and natural) with climatic and environmental factors (Normalized Difference Vegetation Index (NDVI), Normalized Difference Water Index (NDWI), Land Surface Temperature (LST) and precipitation). We show that the relative abundance of questing nymphs was significantly associated with climatic conditions, such as higher values of NDVI recorded in the sampling period, while no differences were observed among land use categories. However, the density of infected nymphs (DIN) also depended on the pathogen considered and land use. These results contribute to a better understanding of the variation in acarological hazard for Ixodes ricinus transmitted pathogens in Central Europe and provide the basis for more focused ecological studies aimed at assessing the effect of land use in different sites on tick-host pathogens interaction.

Keywords: Anaplasma phagocytophilum; Borrelia burgdorferi sensu lato; Rickettsia spp.; acarological hazard; density of infected nymphs; land use; normalized difference vegetation index.

Figure 1

Map of the 19 ticks sampling sites in Italy, Germany, Czech Republic, Slovakia and Hungary (see Table 1).

Figure 2

Boxplot of observed questing I. ricinus nymphs collected over the year (April–May–June period) in different countries and habitat types; x-axis = country; y-axis = number of collected nymphs.

Figure 3

Best models for questing nymph density (Negative Binomial Generalized Linear Mixed Model); values on the x-axis represent the mean normalized difference vegetation index (NDVI) over three months (April, May, June); values on the y-axis represent the number of collected nymphs. The solid black line represents the fitted values (highlighting the relationship between NDVI and the typical country-year) computed by considering the accumulated precipitation in the 4th quarter at its mean value. Dashed lines are the 95% confidence intervals for the fitted values. Coloured lines represent the association between the number of collected nymphs and NDVI within each country. Points are observed values.

Figure 4

Best Linear Mixed Models for density of infected nymphs (DIN) for A. phagocytophilum (left panel), B. burgdorferi s.l. (central panel), Rickettsia spp. (right panel). Filled circles represent the fitted values, and empty circles are the observed values. Solid lines represent the 95% confidence intervals for the fitted values.