Spatial and temporal variation of five different pathogens and symbionts in Ixodes ricinus nymphs in the Netherlands

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Abstract

The incidence of diseases caused by pathogens transmitted by the tick Ixodes ricinus vary over time and space through incompletely understood mechanisms. An important determinant of the disease risk is the density of infected ticks, which is the infection prevalence times the density of questing ticks. We therefore investigated the spatial and temporal variation of four pathogens and one of the most abundant symbionts in Ixodes ricinus in questing nymphs over four years of monthly collections in 12 locations in the Netherlands. The infection prevalence of all microbes showed markedly different patterns with significant spatial variation for Borrelia burgdorferi (s.l.), Neoehrlichia mikurensis, Rickettsia helvetica, and Midichloria mitochondrii, significant seasonal variation of B. burgdorferi (s.l.), N. mikurensis, and M. mitochondrii and a significant interannual variation of R. helvetica. Despite its ubiquitous presence, no spatio-temporal variation was observed for the infection prevalence of B. miyamotoi. The variation in infection prevalence was generally smaller than the variation in the density of nymphs, which fluctuated substantially both seasonally and between locations. This means that the variation in the densities of infected nymphs for all pathogens was mostly the result of the variation in densities of nymphs. We also investigated whether there were positive or negative associations between the symbionts, and more specifically whether ticks infected with vertically transmitted symbionts like M. mitochondrii and R. helvetica, have a higher prevalence of horizontally transmitted symbionts, such as B. burgdorferi (s.l.) and N. mikurensis. We indeed found a clear positive association between M. mitochondrii and B. burgdorferi (s.l.). The positive association between R. helvetica and B. burgdorferi (s.l.) was less clear and was only shown in two locations. Additionally, we found a clear positive association between B. burgdorferi (s.l.) and N. mikurensis, which are both transmitted by rodents. Our longitudinal study indicated strong between-location variation, some seasonal patterns and hardly any differences between years for most symbionts. Positive associations between symbionts were observed, suggesting that infection with a (vertically transmitted) symbiont may influence the probability of infection with other symbionts, or that there is a common underlying mechanism (e.g. feeding on rodents).

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荷兰蓖麻线虫若虫体内五种不同病原体和共生体的时空变化
由蜱虫传播的病原体所引起的疾病的发病率会随着时间和空间的变化而变化,其机制尚不完全清楚。疾病风险的一个重要决定因素是受感染蜱虫的密度,即感染率乘以寻蜱密度。因此,我们在荷兰的 12 个地点,通过四年的每月采集,研究了蓖麻介壳虫若虫中四种病原体和一种最丰富的共生体的时空变化。所有微生物的感染率都显示出明显不同的模式,其中包柔氏菌(s.l.)、米库雷氏新立克次体(Neoehrlichia mikurensis)、螺旋立克次体(Rickettsia helvetica)和线粒体敌敌畏(Midichloria mitochondrii)有显著的空间变化,包柔氏菌(s.l.)、米库雷氏新立克次体(Neoehrlichia mikurensis)和线粒体敌敌畏(M. mitochondrii)有显著的季节变化,螺旋立克次体(R. helvetica)有显著的年际变化。尽管宫本线虫无处不在,但其感染率没有时空变化。感染率的变化一般小于若虫密度的变化,若虫密度在季节和地点之间都有很大波动。这说明所有病原体感染若虫密度的变化主要是由若虫密度的变化造成的。我们还研究了共生体之间是否存在正或负的联系,更具体地说,研究了感染线粒体和螺旋体等垂直传播共生体的蜱虫是否会感染更多的水平传播共生体,如B. burgdorferi(s.l.)和N. mikurensis。我们确实发现线粒体与 B. burgdorferi(s.l.)之间存在明显的正相关。而 R. helvetica 与 B. burgdorferi(s.l.)之间的正相关性则不太明显,而且只在两个地方出现。此外,我们还发现 B. burgdorferi(s.l.)与 N. mikurensis(均由啮齿动物传播)之间存在明显的正相关。我们的纵向研究表明,大多数共生体在不同地点之间有很大的差异,有一些季节性模式,而在不同年份之间几乎没有差异。共生体之间存在正相关关系,这表明感染一种(垂直传播的)共生体可能会影响感染其他共生体的概率,或者存在一种共同的潜在机制(例如以啮齿动物为食)。
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