Masting by beech trees predicts the risk of Lyme disease

Abstract

Background The incidence of Lyme borreliosis and other tick-borne diseases is increasing in Europe and North America. There is currently much interest in identifying the ecological factors that determine the density of infected ticks as this variable determines the risk of Lyme borreliosis to vertebrate hosts, including humans. Lyme borreliosis is caused by the bacterium Borrelia burgdorferi sensu lato (s.l.) and in western Europe, the hard tick Ixodes ricinus is the most important vector. Methods Over a 15-year period (2004–2018), we monitored the monthly abundance of I. ricinus ticks (nymphs and adults) and their B. burgdorferi s.l. infection status at four different elevations on a mountain in 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 2 years after a masting event. We used generalized linear mixed effects models and AIC-based model selection to identify the ecological factors that influence inter-annual variation in the nymphal infection prevalence (NIP) and the density of infected nymphs (DIN). Results We found that the NIP decreased by 78% over the study period. Inter-annual variation in the NIP 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, and the decrease was significant at the top elevation. Inter-annual variation in the DIN was best explained by elevation site, year, beech tree masting index 2 years prior and the mean relative humidity in the present year. This is the first study in Europe to demonstrate that seed production by deciduous trees influences the density of nymphs infected with B. burgdorferi s.l. and hence the risk of Lyme borreliosis. Conclusions Public health officials in Europe should be aware that masting by deciduous trees is an important predictor of the risk of Lyme borreliosis.

Beech tree masting explains the inter-annual variation in the fall and spring peaks ofIxodes ricinusticks with different time lags

“…Thus, for each climate variable, there were a total of 12 seasonal means (3 years * 4 seasons per year = 12) and 3 annual means. The exception was the annual snow fall (units of cm) which was calculated over the time from October 1 (e.g., previous year) to May 31. Annual beech masting score: Previous studies have shown that there is a 2-year time lag between masting events and the annual DON and the annual DIN [12,14,35,36]. Our recent analyses of the same data showed that inter-annual variation in the DON and the DIN was strongly associated with the mast scores 2 years prior of European beech but not Norway spruce [12,36].…”

“…Given the importance of I. ricinus as a disease vector, forecasting the density of ticks questing for hosts is important for managing the risk of tick-borne diseases [12,13,35,36,[69][70][71]. In Europe, there is much interest to determine which ecological factors are influencing the seasonal and inter-annual abundance of I. ricinus ticks [12,35].…”

“…An interesting result of our study was that the seasonal climate variables were much more important than the annual climate variables at explaining the inter-annual variation in the DON. Our previous work found that annual climate variables (e.g., mean annual relative humidity and mean annual precipitation) were important for explaining the inter-annual variation in the DON or DIN [12,36], but these studies did not investigate seasonal means. The present study is better because it compares climate variables operating at different temporal scales (i.e., annual versus seasonal).…”

“…Studies on I. ricinus in Europe and on I. scapularis in North America have shown that interannual variation in seed production by deciduous trees drives inter-annual variation in the density of nymphs 2 years later; this relationship is mediated by rodents that feed on the tree seeds and provide blood meals for the larvae [12,14,15,[32][33][34][35][36]. In summary, masting in the fall of year y-2 enhances rodent density and larval feeding success in the spring and summer of year y-1, which increases the density of nymphs in year y.…”

The ecology and evolution of synchronized reproduction in long-lived plants

“…For example, forecasts of seed and fruit crops in New Zealand inform both the management of invasive mammals and translocation programmes of the endangered kakapo [ 95,96]. Similarly, the effect of masting on zoonotic, tick-borne disease incidents in human populations, driven by the effect of cycling rodent populations on tick numbers, can be forecast with a time horizon of up to 2 years [97]. In other cases, where forecasts of seed and fruit crops are not made, interannual variation in seed crops is an obstacle to environmental management.…”