Microbiomes of soils and plants are linked, but how this affects microbiomes of aboveground herbivorous insects is unknown. We first generated plant-conditioned soils in field plots, then reared leaf-feeding caterpillars on dandelion grown in these soils, and then assessed whether the microbiomes of the caterpillars were attributed to the conditioned soil microbiomes or the dandelion microbiome. Microbiomes of caterpillars kept on intact plants differed from those of caterpillars fed detached leaves collected from plants growing in the same soil. Microbiomes of caterpillars reared on detached leaves were relatively simple and resembled leaf microbiomes, while those of caterpillars from intact plants were more diverse and resembled soil microbiomes. Plant-mediated changes in soil microbiomes were not reflected in the phytobiome but were detected in caterpillar microbiomes, however, only when kept on intact plants. Our results imply that insect microbiomes depend on soil microbiomes, and that effects of plants on soil microbiomes can be transmitted to aboveground insects feeding later on other plants.

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There is increasing evidence that a mass extinction event is in its early stages across much of the biosphere (Ceballos et al., 2017; Dirzo et al., 2014; Pievani, 2014). Well-studied species (vascular plants, vertebrates) have lost as much as 60% of genetic diversity over the past 50 years alone (Ripple et al., 2017). Recent studies are reporting that terrestrial insect biomass and/or diversity are also declining in some re

Plant-soil feedbacks are shaped by microbial legacies that plants leave in the soil. We tested the persistence of these legacies after subsequent colonization by the same or other plant species using 6 typical grassland plant species. Soil fungal legacies were detectable for months, but the current plant effect on fungi amplified in time. By contrast, in bacterial communities, legacies faded away rapidly and bacteria communities were influenced strongly by the current plant. However, both fungal and bacterial legacies were conserved inside the roots of the current plant species and their composition significantly correlated with plant growth. Hence, microbial soil legacies present at the time of plant establishment play a vital role in shaping plant growth even when these legacies have faded away in the soil due the growth of the current plant species. We conclude that soil microbiome legacies are reversible and versatile, but that they can create plant-soil feedbacks via altering the endophytic community acquired during early ontogeny.

Soil legacy effects are commonly highlighted as drivers of plant community dynamics and species co-existence. However, experimental evidence for soil legacy effects of conditioning plant communities on responding plant communities under natural conditions is lacking. We conditioned 192 grassland plots using six different plant communities with different ratios of grasses and forbs and for different durations. Soil microbial legacies were evident for soil fungi, but not for soil bacteria, while soil abiotic parameters did not significantly change in response to conditioning. The soil legacies affected the composition of the succeeding vegetation. Plant communities with different ratios of grasses and forbs left soil legacies that negatively affected succeeding plants of the same functional type. We conclude that fungal-mediated soil legacy effects play a significant role in vegetation assembly of natural plant communities. and robin.heinen@tum.de † These authors contributed equally to this work.

Our findings highlight how soil fungal and bacterial communities respond to time, season, and plant species identity. We found that succession shapes the soil bacterial community, while plant species and the type of plant species that grows in the soil drive the assembly of soil fungal communities. Future research on the effects of plants on soil microbes should take into consideration the relative roles of both time and plant growth on creating soil legacies that impact future plants growing in the soil. Understanding the temporal (in)stability of microbial communities in soils will be crucial for predicting soil microbial composition and functioning, especially as plant species compositions will shift with global climatic changes and land-use alterations. As fungal and bacterial communities respond to different environmental cues, our study also highlights that the selection of study organisms to answer specific ecological questions is not trivial and that the timing of sampling can greatly affect the conclusions made from these studies.

Abstract1. Plants leave species-specific legacies in the soil they grow in that can represent changes in abiotic or biotic soil properties. It has been shown that such legacies can affect future plants that grow in the same soil (plant-soil feedback, PSF). Such processes have been studied in detail, but mostly on individual plants. Here, we study PSF effects at the community level and use a trait-based approach both in the conditioning phase and in the feedback phase to study how 12 individual soil legacies influence six plant communities that differ in root size.2. We tested if (1) grassland perennial species with large root systems would leave a stronger legacy than those with small root systems, (2) grass species would leave a more positive soil legacy than forbs, and (3) communities with large root systems would be more responsive than small-rooted communities. We also tested (4) whether a leaf-chewing herbivore and a phloem feeder were affected by soil legacy effects in a community framework.3. Our study shows that the six different plant communities that we used respond differently to soil legacies of 12 different plant species and their functional groups.Species with large root systems did not leave stronger legacies than species with small root systems, nor were communities with large root systems more responsive than communities with root systems.4. Moreover, we show that when communities are affected by soil legacies, these effects carry over to the chewing herbivore Mamestra brassicae (Lepidoptera: Noctuidae) through induced behavioural changes resulting in better performance of a chewing herbivore on forb-conditioned soils than on grass-conditioned soils, whereas performance of the phloem feeder Rhopalosiphum padi (Hemiptera: Aphididae) remained unaffected.5. Synthesis. The results of this study shed light on the variability of soil effects found in previous work on feedbacks in communities. Our study suggests that the composition of plant communities determines to a large part the response to soil legacies.Furthermore, the responses to soil legacies of herbivores feeding on the plant communities that we observed, suggests that in natural ecosystems, the vegetation history may also have an influence on contemporary herbivore assemblages. ThisThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Soil biota-plant interactions play a dominant role in terrestrial ecosystems. Through nutrient mineralization and mutualistic or antagonistic interactions with plants soil biota can affect plant performance and physiology and via this affect plant-associated aboveground insects. There is a large body of work in this field that has already been synthesized in various review papers. However, most of the studies have been carried out under highly controlled laboratory or greenhouse conditions. Here, we review studies that manipulate soil organisms of four dominant taxa (i.e., bacteria, fungi, nematodes, and soil arthropods) in the field and assess the effects on the growth of plants and interactions with associated aboveground insects. We show that soil organisms play an important role in shaping plant-insect interactions in the field and that general patterns can be found for some taxa. Plant growth-promoting rhizobacteria generally have negative effects on herbivore performance or abundance, most likely through priming of defenses in the host plant. Addition of arbuscular mycorrhizal fungi (AMF) has positive effects on sap sucking herbivores, which is likely due to positive effects of AMF on nutrient levels in the phloem. The majority of AMF effects on chewers were neutral but when present, AMF effects were positive for specialist and negative for generalist chewing herbivores. AMF addition has negative effects on natural enemies in the field, suggesting that AMF may affect plant attractiveness for natural enemies, e.g., through volatile profiles. Alternatively, AMF may affect the quality of prey or host insects mediated by plant quality, which may in turn affect the performance and density of natural enemies. Nematodes negatively affect the performance of sap sucking herbivores (generally through phloem quality) but have no effect on chewing herbivores. For soil arthropods there are no clear patterns yet. We further show that the methodology used plays an important role in influencing the outcomes of field studies. Studies using potted plants in the field and studies that remove target soil taxa by means of pesticides are most likely to detect significant results. Lastly, we discuss suggestions for future research that could increase our understanding of soil biota-plant-insect interactions in the field.