Land-use effects on parasite-metazoan host association in soils at a continental scale

Abstract Soils harbor a large number of unicellular eukaryotic parasites. These parasites, such as Apicomplexa, inhabit a wide range of soil metazoans. However, the distribution of these apicomplexan parasites, their links with hosts and the impact of human-dominated land use remain unknown across larger spatial scales. In this study, we used metabarcoding to investigate the biogeography of and links between Apicomplexa and soil metazoa in three human-dominated ecosystem types (farmlands, residential areas and parks) and more natural forests across subtropical, warm-temperate and mid-temperate climatic regions in China. Our results showed that human-dominated land use indirectly reduced apicomplexan taxon richness by reducing metazoan taxon richness. However, the richness reduction of the parasites was more pronounced in the subtropical region than in temperate regions, with the underlying mechanisms also differing among climate regions. While annual precipitation positively linked with apicomplexan richness in forests through increasing metazoan richness, climatic factors were of minor importance in human-dominated ecosystems, because of a decoupling between apicomplexan and metazoan biodiversity. Our study extends the understanding of the biodiversity of soil metazoan parasites from natural to managed systems. We conclude that land use threatens both soil animals and their parasites, with particularly strong effects on parasites in high biodiversity regions. In addition, the parasite-host association is often decoupled due to the anthropogenic modification of ecosystems. Further studies are needed to decipher the functional importance of soil parasites as their reduction in highly managed systems might indirectly affect metazoan functioning.