Dynamics of Ixodes ricinus and associated bacterial pathogens in the forest and agricultural ecosystems of northeastern France

法国东北部森林和农业生态系统中蓖麻硬蜱及其相关细菌病原体的动态变化

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Abstract

Ixodes ricinus ticks evolve mainly in forest ecosystems, which can be affected by human activities in different ways. The present study aimed to analyze the relationship between different landscapes, tick populations, and the circulation of bacterial agents in three French departments, i.e., Ardennes, Marne, and Meuse. A total of eight sites were selected in wetlands, agricultural areas, forest areas, and a hunting park. All these sites host populations of forest rodents, European badger, red fox, and roe deer; some also host wild boar. Ticks were collected during the period of peak activity from March to June over the course of 3 years. Ixodes ricinus nymphs were then analyzed by PCR for the presence of the following bacteria: Borrelia burgdorferi sensu lato, Neoehrlichia mikurensis, Anaplasma phagocytophilum, and Borrelia miyamotoi. The highest tick density, 145.7 nymphs/100 m(2) was observed in the hunting park; specifically, in a specific double-fenced enclosure where the vegetation was particularly abundant with large deciduous trees. The presence of various hosts (rodents, badgers, foxes, and roe deer) was recorded. N. mikurensis and B. burgdorferi s.l., with a prevalence of 11.2% and 9.8%, respectively, were the most detected microorganisms in nymphs. Overall, 25.7% of the tested ticks were positive, and 3.3% carried at least two microorganisms. Forested areas surrounded either by agricultural areas or sites characterized by their host diversity and dense herbaceous vegetation appear suitable for the proliferation of ticks and associated pathogens.IMPORTANCEThe distribution and abundance of Ixodes ricinus ticks and associated pathogens vary according to the ecosystem. Forest areas, characterized by dense vegetation, many large trees, abundant leaf litter, and certain vertebrate hosts, have the highest tick densities. The impact of anthropization on these factors has not been sufficiently studied. In this study, we measured tick abundance in relation to the presence of wild animals (ungulates and rodents) and vegetation data, which are important factors influencing tick proliferation. In addition, we interviewed forestry workers, hunters, and farmers in the study area to identify natural and anthropogenic factors likely to affect tick populations. Overall, we conclude that ecosystem changes, in particular afforestation and deer population expansion, need to be thoroughly assessed in order to develop effective control measures while ensuring climate change mitigation.

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