Collembola communities across forest ecosystems in Germany: Long-term dynamics and interrelationships with fungal food resources

Abstract

Collembola, one of the most abundant animals in soils worldwide, are important drivers of soil ecosystem services such as carbon sequestration and the cycling of organic matter. By feeding on fungal hyphae and spores, they are shaping fungal community structure and dispersal by transporting spores through the gut passage and body surfaces. Trophic niches and thereby feeding preferences are known to depend on Collembola life form and phylogenetic identity. Thus, the community composition of Collembola is an important driver of ecosystem services. Even though it is known that Collembola prefer saprotrophic over ectomycorrhizal fungi, more specific information on Collembola fungivory in natural systems is still lacking. Therefore, the identification of Collembola community composition and abundance and knowledge on Collembola diets is crucial for understanding soil ecosystem functioning. We established a comprehensively tested and standardized method for the decontamination of Collembola body surfaces for the use in DNA-based analysis of trophic interactions in soil microarthropods (Chapter 2). In this study, we identified chlorine bleach (Sodium hypochloride, NaClO; 5 % for Acari; 1.5 % for Collembola) to be most efficient in decreasing fungal surface contaminants by at least 80 % without harming the detection of ingested prey material. Further, we analyzed the gut content and possible gut symbionts of six Collembola species, Ceratophysella denticulata, Isotomiella minor, Lepidocyrtus lanuginosus, Folsomia quadrioculata, Paristoma notabilis and Protaphorura armata, of beech and spruce forests (Chapter 3). Targeted amplicon sequencing of the ITS2 gene fragment was used to identify a broad spectrum of ingested fungal genera. No indications for fungal gut symbionts were detected in starved Collembola. Unexpectedly, the composition of the fungal genera identified in the gut of Collembola did not differ significantly between spruce and beech forests. Collembola preferred saprotrophic or pathotrophic fungal genera, such as Cladosporium, Ramularia, Mycena and Encoelia over ectomycorrhizal fungi indicating that the latter are of minor importance for Collembola nutrition. Unfortunately, we only obtained a limited number of OTUs assigned to ingested fungal genera, which presumably was caused by the amplification bias of the used primers towards Collembola DNA. In addition, we found evidence of a cuticle infection with the entomopathogenic genus Scopulariopsis in all analyzed Collembola. In a long-term soil fauna monitoring experiment conducted in the framework of the Biodiversity Exploratories, we identified factors affecting Collembola abundance and species composition in a forest management intensity gradient in three regions across Germany (Chapter 4). Samples were taken during spring every three years between 2008 and 2020. Collembola abundances and species richness did not decline with time. However, abundances and community compositions fluctuated with time depending on regional and climatic factors. Variations in Collembola abundances were high in sand-rich soils in the Schorfheide and shallow soils in the Swabian Alb. These soils have lower water holding capacity compared to clay-rich soils in the Hainich, and thus Collembola seem to be strongly affected by drought periods in the former regions. Further, Collembola community composition was affected by the identity of the dominant tree species (coniferous and deciduous), but no significant effect of forest management intensity on Collembola community structure or abundance was detected. Precipitation and microbial biomass were identified as the strongest factor affecting litter dwelling life forms (epedaphic and hemiedaphic) of Collembola, which mainly feed on microbial material. Surprisingly, euedaphic Collembola were not significantly affected by changing climatic conditions or regional specific factors across the study period and sampling sites. However, highest proportions of parthenogenetically reproducing species, among them many euedaphic species, were at a maximum in the Schorfheide indicating that parthenogenetic species are able to recover quickly after harsh environmental disturbances, such as drought. Overall, the results highlight that detrimental effects of weather extremes are less pronounced in regions with clay-rich soils, which facilitate higher soil hydration and nutrition. In conclusion, the results of this thesis suggest that the soil system in temperate forests is well buffered against climatic changes and responds much slower to global climate change than aboveground arthropods. Therefore, more intensive monitoring of a wider range of forest types is needed to investigate long-term changes. Collembola in general seem to be resilient to environmental changes presumably related to their flexibility in using a wide range of food resources and recovering quickly after population declines due to harsh environmental conditions. However, the influence of climate change factors on feeding strategies and nutrition of Collembola and its implications for ecosystem services needs more detailed attention.