Spatiotemporal ecological factors influencing the ecology of "Ixodes ricinus" ticks and the Lyme disease risk
Authors:   , Bregnard Cindy 
Published: May 2022

Ticks and tick-borne diseases represent a significant health problem for humans and their companion animals. Tick-borne pathogens cause morbidity and mortality in their vertebrate hosts (including humans). The incidence of Lyme borreliosis and other tick-borne diseases is increasing in Europe and North America. To predict the risk of tick-borne disease, it is critical to understand the ecological factors that determine the abundance of ticks and the density of infected ticks as this variable determines the risk of Lyme borreliosis to vertebrate hosts including humans. In Europe, the sheep tick (Ixodes ricinus) transmits a number of important diseases including Lyme borreliosis, which is caused by the bacterium Borrelia burgdorferi sensu lato (sl). In continental Europe, the nymphal stage of I. ricinus often has a bimodal phenology with a large spring peak and a smaller fall peak. There is consensus about the origin of the spring nymphal peak, but the origin of the fall nymphal peak remains unclear. Two alternative hypotheses predict different time lags (0 year versus 1 year) between the fall peak of the nymphal ticks and the blood meal of the previous stage (larval tick). The feeding success of the larval ticks depends on the density of their small mammal hosts, which in turn, depends on the seed production (masting) by deciduous trees. This PhD thesis aimed to determine the abiotic and biotic factors that influence the seasonal and inter-annual variation in the density of nymphs (DON) and density of infected nymphs (DIN) at a location in Switzerland where Lyme borreliosis is endemic. Over a 15-year period (2004 to 2018), we monitored the monthly abundance of I. ricinus ticks (nymphs and adults) and their B. burgdorferi sl infection status at four different elevations on Chaumont Mountain in Neuchâtel, western Switzerland. We collected climate variables in the field and from nearby weather stations. We obtained data on beech tree seed production (masting) from the literature, as the abundance of Ixodes nymphs can increase dramatically two years after a masting event. We used generalized linear models and AIC-based model selection to identify the ecological factors that influence inter-annual variation in the DON, DIN and, the nymphal infection prevalence (NIP). We used generalized additive models and AIC-based model selection to model the complex bimodal seasonal phenology of I. ricinus nymphs and whether this approach yields additional insights into the factors that explain seasonal variation in tick abundance. In chapter 1, we found that elevation, year, masting events two years prior, and relative humidity together explained 73.2% of the variation in our annual estimates of the DON. According to the parameter estimates of our models, (i) the annual density of nymphs almost doubled over the 15-year study period, (ii) changing the beech tree seed production index from 1 to 5 increased the abundance of nymphs by 86.2% two years later, and (iii) increasing the field-collected relative humidity from 50.0% to 75.0% decreased the abundance of nymphs by 46.4% in the same year. In chapter 2, we found that the inter-annual variation in the NIP decreased by 78% over the study period and was explained by the mean precipitation in the present year, and the duration that the DNA extraction was stored in the freezer prior to pathogen detection. The DIN decreased over the study period at all four elevation sites, but the decrease was only significant at the top elevation. Inter-annual variation in the DIN was best explained by elevation site, year, masting events two years prior, and the mean relative humidity in the present year. In chapter 3, we found that the I. ricinus nymphs had a bimodal phenology at the three lower elevation sites, but a unimodal phenology at the top elevation site. We also found that the inter-annual variation in the densities of I. ricinus nymphs in the fall and spring were best explained by a 1-year versus a 2-year time lag with the beech tree masting index. The direct development hypothesis is the best explanation for the fall peak of I. ricinus nymphs at our study site. Our study provides new insight into the complex bimodal phenology of this important disease vector. This PhD thesis demonstrated that masting events by deciduous trees is a critical driver of the seasonal and inter-annual abundance of I. ricinus ticks, and hence the risk of tick-borne disease. This work provides new information on the bimodal phenology of I. ricinus ticks, particularly that the direct development hypothesis is the best explanation for the spring and fall peaks of I. ricinus nymphs.