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Most of Earth's trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earth's land plants associate with bacteria that help them survive in nature. Yet, our understanding of how the presence of EcMF modifies soil bacterial communities, soil food webs, and root chemistry requires direct experimental evidence to comprehend the effects that EcMF may generate in the belowground plant microbiome. To this end, we grew Pinus muricata plants in soils that were either inoculated with EcMF and native forest bacterial communities or only native bacterial communities. We then profiled the soil bacterial communities, applied metabolomics and lipidomics, and linked omics data sets to understand how the presence of EcMF modifies belowground biogeochemistry, bacterial community structure, and their functional potential. We found that the presence of EcMF (i) enriches soil bacteria linked to enhanced plant growth in nature, (ii) alters the quantity and composition of lipid and non-lipid soil metabolites, and (iii) modifies plant root chemistry toward pathogen suppression, enzymatic conservation, and reactive oxygen species scavenging. Using this multi-omic approach, we therefore show that this widespread fungal symbiosis may be a common factor for structuring soil food webs.IMPORTANCEUnderstanding how soil microbes interact with one another and their host plant will help us combat the negative effects that climate change has on terrestrial ecosystems. Unfortunately, we lack a clear understanding of how the presence of ectomycorrhizal fungi (EcMF)-one of the most dominant soil microbial groups on Earth-shapes belowground organic resources and the composition of bacterial communities. To address this knowledge gap, we profiled lipid and non-lipid metabolites in soils and plant roots, characterized soil bacterial communities, and compared soils amended either with or without EcMF. Our results show that the presence of EcMF changes soil organic resource availability, impacts the proliferation of different bacterial communities (in terms of both type and potential function), and primes plant root chemistry for pathogen suppression and energy conservation. Our findings therefore provide much-needed insight into how two of the most dominant soil microbial groups interact with one another and with their host plant.

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Ticks (Family Ixodidae) spend most of their life cycle as immature stages in the soil and litter, and as any other soil invertebrates, are likely to be controlled top-down by soil-dwelling predators. To date, the ability of soil invertebrate predators to control ixodid tick population remains little known, partly due to methodological difficulties. In the current study, we developed and successfully tested a novel method of labeling live Ixodes ricinus (L., 1758) (Ixodida: Ixodidae) nymphs with a 15N isotope label. Labeled ticks were used in a small-scale 8-day-long microcosm experiment to reveal soil predators attacking nymphs. Only a small fraction (4.1% of all samples) of soil generalist predators preyed upon nymphs. A strong 15N label was found in 5 predator species, namely 2 spiders (Pachygnatha listeri Sundevall, 1830, Tetragnathidae and Ozyptila sp., Theridiidae), 2 gamasid mites (Pergamasus beklemischevi Sellnick, 1929 and Pergamasus quisquiliarum [Canestrini, 1882], Parasitidae), and 1 staphylinid beetle (Geostiba circellaris [Gravenhorst, 1806], Staphylinidae). The isotopic labeling can be a useful tool in revealing a range of invertebrate predators that can control tick populations in soil.

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Mycorrhizal fungi represent a potentially abundant carbon resource for soil animals, but their role in soil food webs remains poorly understood. To detect taxa that are trophically linked to the extraradical mycelium of mycorrhizal fungi, we used stable isotope (13C) labelling of whole trees in combination with the in-growth mesh bag technique in two coniferous forests. This allowed us to detect the flux of carbon in the mycelium of mycorrhizal fungi, and consequently in the tissues of soil invertebrates. The mycorrhizal fungal genera constituted 93.5% of reads in mycelium samples from the in-growth mesh bags. All mycelium from in-growth mesh bags and about 32% of the invertebrates sampled (in total 11 taxa) received the 13C label after 45 days of exposure. The extent of feeding of soil invertebrates on the mycelium of mycorrhizal fungi depended on the taxonomic affinity of the animals. The strongest trophic link to the mycorrhiza-derived carbon was detected in Isotomidae (Collembola) and Oppiidae (Oribatida). The label was also observed in the generalist predators, indicating the propagation of mycorrhiza-derived carbon into the higher trophic levels of the soil food web. Higher 13C labelling in the tissues of euedaphic Collembola and Oribatida compared to atmobiotic and hemiedaphic families indicates the importance of mycorrhizal fungi as a food resource for invertebrates in deeper soil horizons.

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Changes in land use can generate environmental pressures that influence soil biodiversity, and numerous studies have examined the influences of land use on the soil microbial communities. However, little is known about the effects of land use on ecological interactions of soil microbes and their predators. Diazotrophs are key soil microbes that play important functional roles in fixing atmospheric nitrogen. In this study, we investigated the co-association of diazotroph community members and patterns of diazotroph and bacterivore networks under different long-term land uses including cropland, grassland, and bare land. Diazotroph community was characterized by high-throughput sequencing. The results indicated that land use type influenced the dominant genera of diazotrophs and shaped the occurrence of specific indicator diazotroph taxa. Co-existing pattern analysis of diazotrophs and bacterivores indicated that grassland converted from cropland increased the complexity of diazotroph and bacterivore network structure. The number of nodes for diazotrophs and bacterivores was higher in grassland than in cropland and bare land. Random forest analysis revealed that six bacterivore genera Cephalobus, Protorhabditis, Acrobeloides, Mesorhabditis, Anaplectus, and Monhystera had significant effects on diazotrophs. Bacterivores were found to have predominantly negative effects in bare land. Different bacterivores had differing effects with respect to driving changes in diazotroph community structure. Structural equation model showed that land use could control diazotroph community composition by altering soil properties and regulating abundance of bacterivores. These findings accordingly enhance our current understanding of mechanisms underlying the influence of land use patterns on diazotrophs from the perspective of soil food webs.

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The complex relationship between ecosystem function and soil food web structure is governed by species interactions, many of which remain unmapped. Phagotrophic protists structure soil food webs by grazing the microbiome, yet their involvement in intraguild competition, susceptibility to predator diversity, and grazing preferences are only vaguely known. These species-dependent interactions are contextualized by adjacent biotic and abiotic processes, and thus obfuscated by typically high soil biodiversity. Such questions may be investigated in the McMurdo Dry Valleys (MDV) of Antarctica because the physical environment strongly filters biodiversity and simplifies the influence of abiotic factors. To detect the potential interactions in the MDV, we analyzed the co-occurrence among shotgun metagenome sequences for associations suggestive of intraguild competition, predation, and preferential grazing. In order to control for confounding abiotic drivers, we tested co-occurrence patterns against various climatic and edaphic factors. Non-random co-occurrence between phagotrophic protists and other soil fauna was biotically driven, but we found no support for competition or predation. However, protists predominately associated with Proteobacteria and avoided Actinobacteria, suggesting grazing preferences were modulated by bacterial cell-wall structure and growth rate. Our study provides a critical starting-point for mapping protist interactions in native soils and highlights key trends for future targeted molecular and culture-based approaches.

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Quantitative fatty acid signature analysis (QFASA) as a biochemical tool to study the diet composition of predators is frequently used in marine ecology to infer trophic links in vertebrate consumers. However, the potential and challenges of this method in other ecosystems have only recently been studied. The application in soil ecosystems leads to hurdles not encountered in the marine, such as the low similarity of fatty acid signatures between resource and consumer. So far, diet estimation attempts have been semisuccessful, necessitating to adapt QFASA for use in soil food webs. Dietary fat content may play an important role, as it influences consumer metabolism, and thus calibration coefficients for fatty acid trophic transfer. A series of feeding trials with baker's yeast spiked with five different pure fatty acids at various concentrations was conducted with Collembola, and the changes in calibration coefficients were observed. From there, equations were gained through regression analysis and new sets of calibration coefficients were calculated. QFASA was applied on a range of basal resources and the results compared with previously defined calibration coefficients. Calibration coefficients changed with the proportion of fatty acids in the diet and differed between the three Collembolan species. The re-estimation of diets showed an improvement of model performance by the new calibration coefficients and indicated several modes of fatty acid assimilation. These greatly influence the outcome of diet estimation, for example, algal and bacterial diets are likely underestimated due to high metabolic turnover rates. The application of QFASA in soil ecosystems remains challenging. The variation in calibration coefficients and the resulting decrease in estimation deviation indicate the merit of calculating calibration coefficients from consumer signatures through linear or exponential equations. Ideally, the method should, when extended to the entire fatty acid signature, allow correct determination of consumer diets in soil food webs.

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Standing dead trees (snags) decompose more slowly than downed dead wood and provide critical habitat for many species. The rate at which snags fall therefore influences forest carbon dynamics and biodiversity. Fall rates correlate strongly with mean annual temperature, presumably because warmer climates facilitate faster wood decomposition and hence degradation of the structural stability of standing wood. These faster decomposition rates coincide with turnover from fungal-dominated wood decomposer communities in cooler forests to codomination by fungi and termites in warmer regions. A key question for projecting forest dynamics is therefore whether temperature effects on wood decomposition arise primarily because warmer conditions facilitate faster decomposer metabolism, or are also influenced indirectly by belowground community turnover (e.g., termites exert additional influence beyond fungal-plus-bacterial mediated decomposition). To test between these possibilities, we simulate standing dead trees with untreated wooden posts and follow them in the field across 5 yr at 12 sites, before measuring buried, soil-air interface and aerial post sections to quantify wood decomposition and organism activities. High termite activities at the warmer sites are associated with rates of postfall that are three times higher than at the cooler sites. Termites primarily consume buried wood, with decomposition rates greatest where termite activities are highest. However, where higher microbial and termite activities co-occur, they appear to compensate for one another first, and then to slow decomposition rates at their highest activities, suggestive of interference competition. If the range of microbial and termite codomination of wood decomposer communities expands under climate warming, our data suggest that expansion will accelerate snag fall with consequent effects on forest carbon cycling and biodiversity in forests previously dominated by microbial decomposers.

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To investigate the structural changes of a food-web architecture, we considered real data coming from a soil food web in one abandoned pasture with former low-pressure agriculture management and we reproduced the corresponding ecological network within a multi-agent fully programmable modeling environment in order to simulate dynamically the cascading effects due to the removal of entire functional guilds.We performed several simulations differing from each other for the functional implications. At the first trophic level, we simulated a removal of the prey, that is, herbivores and microbivores, while at the second trophic level, we simulated a removal of the predators, that is, omnivores and carnivores. The five main guilds were removed either separately or in combination.The alteration in the food-web architecture induced by the removal of entire functional guilds was the highest when the entire second trophic level was removed, while the removal of all microbivores caused an alteration in the food-web structure of less than 5% of the total changes due to the removal of opportunistic and predatory species.Omnivores alone account for the highest shifts in time of the numerical abundances of the remaining species, providing computational evidence of the importance of the degree of omnivory in the stabilization of soil biota.

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Soil nitrogen (N) and phosphorus (P) contents, and soil acidification have greatly increased in grassland ecosystems due to increased industrial and agricultural activities. As major environmental and economic concerns worldwide, nutrient enrichment and soil acidification can lead to substantial changes in the diversity and structure of plant and soil communities. Although the separate effects of N and P enrichment on soil food webs have been assessed across different ecosystems, the combined effects of N and P enrichment on multiple trophic levels in soil food webs have not been studied in semiarid grasslands experiencing soil acidification. Here we conducted a short-term N and P enrichment experiment in non-acidified and acidified soil in a semiarid grassland on the Mongolian Plateau. We found that net primary productivity was not affected by N or P enrichment alone in either non-acidified or acidified soil, but was increased by combined N and P enrichment in both non-acidified and acidified soil. Nutrient enrichment decreased the biomass of most microbial groups in non-acidified soil (the decrease tended to be greatest with combined N and P enrichment) but not in acidified soil, and did not affect most soil nematode variables in non-acidified or acidified soil. Nutrient enrichment also changed plant and microbial community structure in non-acidified but not in acidified soil, and had no effect on nematode community structure in non-acidified or acidified soil. These results indicate that the responses to short-term nutrient enrichment were weaker for higher trophic groups (nematodes) than for lower trophic groups (microorganisms) and primary producers (plants). The findings increase our understanding of the effects of nutrient enrichment on multiple trophic levels of soil food webs, and highlight that soil acidification, as an anthropogenic stressor, reduced the responses of plants and soil food webs to nutrient enrichment and weakened plant-soil interactions.

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Shifts in densities of apex predators may indirectly affect fundamental ecosystem processes, such as decomposition, by altering patterns of cascading effects propagating through lower trophic levels. These top-down effects may interact with anthropogenic impacts, such as climate change, in largely unknown ways. We investigated how changes in densities of large predatory arthropods in forest leaf-litter communities altered lower trophic levels and litter decomposition. We conducted our experiment in soil communities that had experienced different levels of long-term average precipitation. We hypothesized that altering abundances of apex predators would have stronger effects on soil communities inhabiting dry forests, due to lower secondary productivity and greater resource overexploitation by lower trophic levels compared to wet forests. We experimentally manipulated abundances of the largest arthropod predators (apex predators) in field mesocosms replicated in the leaf-litter community of Iberian beech forests that differed in long-term mean annual precipitation by 25% (three dry forests with MAP < 1,250 mm and four wet forests with MAP > 1,400 mm). After one year, we assessed abundances of soil fauna in lower trophic levels and indirect impacts on leaf-litter decomposition using litter of understorey hazel, Corylus avellana. Reducing densities of large predators had a consistently negative effect on final abundances of the different trophic groups and several taxa within each group. Moreover, large predatory arthropods strongly impacted litter decomposition, and their effect interacted with the long-term annual rainfall experienced by the soil community. In the dry forests, a 50% reduction in the densities of apex predators was associated with a 50% reduction in decomposition. In wet forests, the same reduction in densities of apex soil predators did not alter the rate of litter decomposition. Our results suggest that predators may facilitate lower trophic levels by indirectly reducing competition and resource overexploitation, cascading effects that may be more pronounced in drier forests where conditions have selected for greater competitive ability and more rapid resource utilization. These findings thus provide insights into the functioning of soil invertebrate communities and their role in decomposition, as well as potential consequences of soil community responses to climate change.

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Earth is experiencing a substantial loss of biodiversity at the global scale, while both species gains and losses are occurring at local and regional scales. The influence of these nonrandom changes in species distributions could profoundly affect the functioning of ecosystems and the essential services that they provide. However, few experimental tests have been conducted examining the influence of species invasions on ecosystem functioning. Even fewer have been conducted using invasive ecosystem engineers, which can have disproportionately strong influence on native ecosystems relative to their own biomass. The invasion of exotic earthworms is a prime example of an ecosystem engineer that is influencing many ecosystems around the world. In particular, European earthworm invasions of northern North American forests cause simultaneous species gains and losses with significant consequences for essential ecosystem processes like nutrient cycling and crucial services to humanity like soil erosion control and carbon sequestration. Exotic earthworms are expected to select for specific traits in communities of soil microorganisms (fast-growing bacteria species), soil fauna (promoting the bacterial energy channel), and plants (graminoids) through direct and indirect effects. This will accelerate some ecosystem processes and decelerate others, fundamentally altering how invaded forests function. This project aims to investigate ecosystem responses of northern North American forests to earthworm invasion. Using a novel, synthetic combination of field observations, field experiments, lab experiments, and meta-analyses, the proposed work will be the first systematic examination of earthworm effects on (1) plant communities and (2) soil food webs and processes. Further, (3) effects of a changing climate (warming and reduced summer precipitation) on earthworm performance will be investigated in a unique field experiment designed to predict the future spread and consequences of earthworm invasion in North America. By assessing the soil chemical and physical properties as well as the taxonomic (e.g., by the latest next-generation sequencing techniques) and functional composition of plant, soil microbial and animal communities and the processes they drive in four forests, work packages I-III take complementary approaches to derive a comprehensive and generalizable picture of how ecosystems change in response to earthworm invasion. Finally, in work package IV meta-analyses will be used to integrate the information from work packages I-III and existing literature to investigate if earthworms cause invasion waves, invasion meltdowns, habitat homogenization, and ecosystem state shifts. Global data will be synthesized to test if the relative magnitude of effects differs from place to place depending on the functional dissimilarity between native soil fauna and exotic earthworms. Moving from local to global scale, the present proposal examines the influence of earthworm invasions on biodiversity-ecosystem functioning relationships from an aboveground-belowground perspective in natural settings. This approach is highly innovative as it utilizes the invasion by exotic earthworms as an exciting model system that links invasion biology with trait-based community ecology, global change research, and ecosystem ecology, pioneering a new generation of biodiversity-ecosystem functioning research.

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The uncertainty of ecological risks and the effects of growing transgenic Bt rice on the environment hamper its commercial production. Here, soil nematode communities were used as an indicator of soil health and soil food web structure to evaluate the potential effects of growing Bt rice without chemical insecticides for 3years in the paddy field. The nematodes and soil physicochemical properties of Bt rice fields were compared to the near-isogenic control, non-Bt rice fields. A total of 108,363 specimens belonging to 28 different genera were enumerated. The Hirschmanniella, Tobrilus, Dorylaimus and Filenchus were dominant genera. A three-year paddy rice cultivation of Bt rice (Huahui 1) negatively affected the abundance of phytoparasitic nematodes but did not affect the total number of nematodes, the abundance and relative abundance of free-living nematodes, genera richness, diversity indices, soil food web conditions, or community compositions. However, apparent seasonal and inter-annual changes in these variables were observed, indicating that the impact of environmental factors was more stronger than that of the Bt toxin. In conclusion, the potential ecological risks of Bt rice on soil health and sustainability warrant further research to disentangle the impacts from various confounding environmental factors.

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We tested experimentally if photoautotrophic microorganisms are a carbon source for invertebrates in temperate soils. We exposed forest or arable soils to a (13)CO2-enriched atmosphere and quantified (13)C assimilation by three common animal groups: earthworms (Oligochaeta), springtails (Hexapoda) and slugs (Gastropoda). Endogeic earthworms (Allolobophora chlorotica) and hemiedaphic springtails (Ceratophysella denticulata) were highly (13)C enriched when incubated under light, deriving up to 3.0 and 17.0%, respectively, of their body carbon from the microbial source in 7 days. Earthworms assimilated more (13)C in undisturbed soil than when the microbial material was mixed into the soil, presumably reflecting selective surface grazing. By contrast, neither adult nor newly hatched terrestrial slugs (Deroceras reticulatum) grazed on algal mats. Non-photosynthetic (13)CO2 fixation in the dark was negligible. We conclude from these preliminary laboratory experiments that, in addition to litter and root-derived carbon from vascular plants, photoautotrophic soil surface microorganisms (cyanobacteria, algae) may be an ecologically important carbon input route for temperate soil animals that are traditionally assigned to the decomposer channel in soil food web models and carbon cycling studies.

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Modern agricultural systems can benefit from the application of concepts and models from applied ecology. When understood, multitrophic interactions among plants, pests, diseases and their natural enemies can be exploited to increase crop production and reduce undesirable environmental impacts. Although the understanding of subterranean ecology is rudimentary compared to the perspective aboveground, technologies today vastly reduce traditional obstacles to studying cryptic communities. Here we emphasize advantages to integrating as much as possible the use of these methods in order to leverage the information gained from studying communities of soil organisms. PCR-based approaches to identify and quantify species (real time qPCR and next generation sequencing) greatly expand the ability to investigate food web interactions because there is less need for wide taxonomic expertise within research programs. Improved methods to capture and measure volatiles in the soil atmosphere in situ make it possible to detect and study chemical cues that are critical to communication across trophic levels. The application of SADIE to directly assess rather than infer spatial patterns in belowground agroecosystems has improved the ability to characterize relationships between organisms in space and time. We review selected methodology and use of these tools and describe some of the ways they were integrated to study soil food webs in Florida citrus orchards with the goal of developing new biocontrol approaches.

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Nematodes are presumably the most numerous Metazoans in terrestrial habitats. They are represented at all trophic levels and are known to respond to nutrient limitation, prey availability, and microbial resources. Predatory nematodes reside at the highest trophic level, and as such their feeding habits could have a major impact on soil food web functioning. Here, we investigate the effects of gender and developmental stage on the nematode body sizes in coarse and loamy soils. Besides Neodiplogasteridae, our predators are much larger than other soil-dwelling nematodes from their early developmental stage onwards. From juvenile to adult, the predatory Aporcelaimellus (Kruskal-Wallis P < 0.001), Dorylaimoides, and Tripyla (both P < 0.01) show great length increases during their developmental growth, in contrast to their possible prey (almost all P < 0.001). Less than 4% of the prey exceeds the length of the predatory adults, but more than 30% of the prey exceeds the length of the predatory juveniles. Potential body size ratios and some physical problems experienced by small fluid feeders attacking large prey are discussed in an attempt to summarize different prey-searching mechanisms and aggregative predatory responses in the soil system.

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As carbon and energy flow through the soil food web they are depleted by the metabolic and production functions of organisms. To be sustained, a "long" food web, with a large biomass at higher trophic levels, must receive a high rate of rhizodeposition or detrital subsidy, or be top-populated by organisms of slow growth and long life cycle. Disturbed soil food webs tend to be bottom heavy and recalcitrant to restoration due to the slow growth of upper predator populations, physical and chemical constraints of the soil matrix, biological imbalances, and the relatively low mobility and invasion potential of soil organisms. The functional roles of nematodes, determined by their metabolic and behavioral activities, may be categorized as ecosystem services, disservices or effect-neutral. Among the disservices attributable to nematodes are overgrazing, which diminishes services of prey organisms, and plant-damaging herbivory, which reduces carbon fixation and availability to other organisms in the food web. Unfortunately, management to ameliorate potential disservices of certain nematodes results in unintended but long-lasting diminution of the services of others. Beneficial roles of nematodes may be enhanced by environmental stewardship that fosters greater biodiversity and, consequently, complementarity and continuity of their services.