Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags

Abstract

Background The tick Ixodes ricinus is an important vector of tick-borne diseases including Lyme borreliosis. 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 there are two alternative hypotheses for the fall nymphal peak. In the direct development hypothesis, larvae quest as nymphs in the fall of the same year that they obtained their larval blood meal. In the developmental diapause hypothesis, larvae overwinter in the engorged state and quest as nymphs one year after they obtained their larval blood meal. These two hypotheses make different predictions about the time lags that separate the larval blood meal and the density of questing nymphs (DON) in the spring and fall. Methods Inter-annual variation in seed production (masting) by deciduous trees is a time-lagged index for the density of vertebrate hosts (e.g., rodents) which provide blood meals for larval ticks. We used a long-term data set on the masting of the European beech tree and a 15-year study on the DON at 4 different elevation sites in western Switzerland to differentiate between the two alternative hypotheses for the origin of the fall nymphal peak. Results Questing I. ricinus nymphs had a bimodal phenology at the three lower elevation sites, but a unimodal phenology at the top elevation site. At the lower elevation sites, the DON in the fall was strongly correlated with the DON in the spring of the following year. The inter-annual variation in the densities of I. ricinus nymphs in the fall and spring was best explained by a 1-year versus a 2-year time lag with the beech tree masting index. Fall nymphs had higher fat content than spring nymphs indicating that they were younger. All these observations are consistent with the direct development hypothesis 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. Conclusions Public health officials in Europe should be aware that following a strong mast year, the DON will increase 1 year later in the fall and 2 years later in the spring. Studies of I. ricinus populations with a bimodal phenology should consider that the spring and fall peak in the same calendar year represent different generations of ticks. Graphical Abstract

Meteorological and climatic variables predict the phenology of Ixodes ricinus nymph activity in France, accounting for habitat heterogeneity

“…The overall phenological patterns observed in our study followed a climatic gradient previously reported: (1) a unimodal pattern with a summer peak and a winter pause (Pattern 1) in freezing climates (Karelia, Russia); (2) a bimodal pattern with spring-autumn peaks (Pattern 2) in intermediate climates (European Russia's temperate zone); (3) a unimodal pattern with a late winter peak (Pattern 3) in warmer climates (Algeria) 18 . Also, a similar phenology trend observed in one mountain region in Switzerland was reported to follow an elevation gradient where the spring-autumn bimodal phenology (Pattern 2) shifted to a late-spring unimodal phenology (Pattern 1) at a higher elevation 17 , presumably due to a temperature gradient. A similar climatic trend was observed in Ixodes scapularis nymphs in a study conducted across a large geographic area in the United States, with peak nymph activity occurring in the summer in colder regions, and late spring in warmer regions 55 .…”

“…However, previous studies on the effects of the environment on I. ricinus nymph activities in Europe did not capture all the aforementioned levels of variation. They largely focused on either a short-term period for multiple sites [21][22][23][24] or a long-term period for a few areas [14][15][16][17] . The present study attempted to explore the baseline abundance, seasonal, and inter-annual variations of I. ricinus nymph activity by expanding the observation across a wide range of geographical/climatic areas over a long period, involving a total 27,53 .…”

“…To better understand the relationship between climatic gradient and phenological patterns, we recommend longitudinal studies conducted over large geographic areas to report the phenological pattern of each sampling location separately. Moreover, determining the age of nymphs through fat content analysis has been demonstrated to guide formulating hypotheses about the mechanisms for the population dynamics of each phenological pattern 17 .…”

Seasonality of host-seekingIxodes ricinusnymph abundance in relation to climate

“…Even applied to adult ticks, these curves can be compared to our predictions for the nymphal stage in Carquefou and Gardouch (oceanic and southwestern basin climate respectively), and in Saint-Genès-Champanelle (mountain climate), respectively. Concerning mountain climate, Bregnard et al (2021a) show a cline ranging from bimodal to unimodal curves when reaching higher altitude (altitude ranging from 620 to 1073 m). According to Gray et al (2016), I. ricinus abundance patterns for larvae, nymphs and adults follow a bimodal curve in Central and Western Europe, but these authors also point out that there are variations on this expert-based pattern.…”

“…mountain climate), respectively. Concerning mountain climate,Bregnard et al (2021a) show a cline ranging from bimodal to unimodal curves when reaching higher altitude (altitude ranging from 620 to 1073 m). According toGray et al (2016), I. ricinus abundance patterns for larvae, nymphs and adults follow a bimodal curve in Central and Western Europe, but these authors also point out that there are variations on this expert-based pattern.…”