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 spri...

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Autores principales:	Cindy Bregnard, Olivier Rais, Coralie Herrmann, Olaf Kahl, Katharina Brugger, Maarten J. Voordouw
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Beech tree Bimodal phenology Climate Diapause Ixodes ricinus Fagus sylvatica Infectious and parasitic diseases RC109-216
Acceso en línea:	https://doaj.org/article/31d1ca2869c744f8b6babe9fee4733d5
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spelling	oai:doaj.org-article:31d1ca2869c744f8b6babe9fee4733d52021-11-14T12:25:14ZBeech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags10.1186/s13071-021-05076-81756-3305https://doaj.org/article/31d1ca2869c744f8b6babe9fee4733d52021-11-01T00:00:00Zhttps://doi.org/10.1186/s13071-021-05076-8https://doaj.org/toc/1756-3305Abstract 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 AbstractCindy BregnardOlivier RaisCoralie HerrmannOlaf KahlKatharina BruggerMaarten J. VoordouwBMCarticleBeech treeBimodal phenologyClimateDiapauseIxodes ricinusFagus sylvaticaInfectious and parasitic diseasesRC109-216ENParasites & Vectors, Vol 14, Iss 1, Pp 1-26 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Beech tree Bimodal phenology Climate Diapause Ixodes ricinus Fagus sylvatica Infectious and parasitic diseases RC109-216
spellingShingle	Beech tree Bimodal phenology Climate Diapause Ixodes ricinus Fagus sylvatica Infectious and parasitic diseases RC109-216 Cindy Bregnard Olivier Rais Coralie Herrmann Olaf Kahl Katharina Brugger Maarten J. Voordouw Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags
description	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
format	article
author	Cindy Bregnard Olivier Rais Coralie Herrmann Olaf Kahl Katharina Brugger Maarten J. Voordouw
author_facet	Cindy Bregnard Olivier Rais Coralie Herrmann Olaf Kahl Katharina Brugger Maarten J. Voordouw
author_sort	Cindy Bregnard
title	Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags
title_short	Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags
title_full	Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags
title_fullStr	Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags
title_full_unstemmed	Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags
title_sort	beech tree masting explains the inter-annual variation in the fall and spring peaks of ixodes ricinus ticks with different time lags
publisher	BMC
publishDate	2021
url	https://doaj.org/article/31d1ca2869c744f8b6babe9fee4733d5
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Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags

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