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Soils contain biotic and abiotic legacies of previous conditions that may influence plant community biomass and associated aboveground biodiversity. However, little is known about the relative strengths and interactions of the various belowground legacies on aboveground plant-insect interactions. We used an outdoor mesocosm experiment to investigate the belowground legacy effects of range-expanding versus native plants, extreme drought and their interactions on plants, aphids and pollinators. We show that plant biomass was influenced more strongly by the previous plant community than by the previous summer drought. Plant communities consisted of four congeneric pairs of natives and range expanders, and their responses were not unanimous. Legacy effects affected the abundance of aphids more strongly than pollinators. We conclude that legacies can be contained as soil 'memories' that influence aboveground plant community interactions in the next growing season. These soil-borne 'memories' can be altered by climate warming-induced plant range shifts and extreme drought.
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Afídeos , Solo , Animais , Secas , Insetos , Biomassa , Plantas , EcossistemaRESUMO
Climate change is causing range shifts of many species to higher latitudes and altitudes and increasing their exposure to extreme weather events. It has been shown that range-shifting plant species may perform differently in new soil than related natives; however, little is known about how extreme weather events affect range-expanding plants compared to related natives. In this study we used outdoor mesocosms to study how range-expanding plant species responded to extreme drought in live soil from a habitat in a new range with and without live soil from a habitat in the original range (Hungary). During summer drought, the shoot biomass of the range-expanding plant community declined. In spite of this, in the mixed community, range expanders produced more shoot biomass than congeneric natives. In mesocosms with a history of range expanders in the previous year, native plants produced less biomass. Plant legacy or soil origin effects did not change the response of natives or range expanders to summer drought. During rewetting, range expanders had less biomass than congeneric natives but higher drought resilience (survival) in soils from the new range where in the previous year native plant species had grown. The biomass patterns of the mixed plant communities were dominated by Centaurea spp.; however, not all plant species within the groups of natives and of range expanders showed the general pattern. Drought reduced the litter decomposition, microbial biomass, and abundances of bacterivorous, fungivorous, and carnivorous nematodes. Their abundances recovered during rewetting. There was less microbial and fungal biomass, and there were fewer fungivorous nematodes in soils from the original range where range expanders had grown in the previous year. We concluded that in mixed plant communities of range expanders and congeneric natives, range expanders performed better, under both ambient and drought conditions, than congeneric natives. However, when considering the responses of individual species, we observed variations among pairs of congenerics, so that under the present mixed-community conditions there was no uniformity in responses to drought of range expanders versus congeneric natives. Range-expanding plant species reduced soil fungal biomass and the numbers of soil fungivorous nematodes, suggesting that the effects of range-expanding plant species can trickle up in the soil food web.
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Plants allocate resources to processes related to growth and enemy defence. Simultaneously, they interact with complex soil microbiomes that also affect plant performance. While the influence of individual microbial groups on single plants is increasingly studied, effects of microbial interactions on growth, defence and growth-defence relationships remain unknown, especially at the plant community level. We investigated how three microbial groups (bacteria, fungi, protists), alone and in full-factorial combinations, affect plant performance and potential growth-defence relationships by measuring phenolics composition in early- and mid-successional grass and forb communities in a glasshouse experiment. Microbial groups did not affect plant growth and only fungi increased defence compounds in early- and mid-successional forbs, while grasses were not affected. Shoot biomass-defence relationships were negatively correlated in most microbial treatments in early-successional forbs, but positively in several microbial treatments in mid-successional forbs. The growth-defence relationship was generally negative in early-successional but not in mid-successional grasses. The presence of different microbiomes commonly removed the observed growth-defence relationships. We conclude that soil microorganisms and their interactions can shift growth-defence relationships differentially for plant functional groups and the relationships vary between successional stages. Microbial interaction-induced growth-defence shifts might therefore underlie distinct plant strategies and fitness.
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Microbiologia do Solo , Solo , Fungos , Interações Microbianas , PlantasRESUMO
It is generally assumed that the dependence of conventional agriculture on artificial fertilizers and pesticides strongly impacts the environment, while organic agriculture relying more on microbial functioning may mitigate these impacts. However, it is not well known how microbial diversity and community composition change in conventionally managed farmers' fields that are converted to organic management. Here, we sequenced bacterial and fungal communities of 34 organic fields on sand and marine clay soils in a time series (chronosequence) covering 25 years of conversion. Nearby conventional fields were used as references. We found that community composition of bacteria and fungi differed between organic and conventionally managed fields. In the organic fields, fungal diversity increased with time since conversion. However, this effect disappeared when the conventional paired fields were included. There was a relationship between pH and soil organic matter content and the diversity and community composition of bacteria and fungi. In marine clay soils, when time since organic management increased, fungal communities in organic fields became more dissimilar to those in conventional fields. We conclude that conversion to organic management in these Dutch farmers' fields did not increase microbial community diversity. Instead, we observed that in organic fields in marine clay when time since conversion increased soil fungal community composition became progressively dissimilar from that in conventional fields. Our results also showed that the paired sampling approach of organic and conventional fields was essential in order to control for environmental variation that was otherwise unaccounted for.
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Agricultura Orgânica , Solo , Agricultura/métodos , Bactérias/genética , Argila , Fungos/genética , Agricultura Orgânica/métodos , Solo/química , Microbiologia do SoloRESUMO
Current climate change has led to latitudinal and altitudinal range expansions of numerous species. During such range expansions, plant species are expected to experience changes in interactions with other organisms, especially with belowground biota that have a limited dispersal capacity. Nematodes form a key component of the belowground food web as they include bacterivores, fungivores, omnivores and root herbivores. However, their community composition under climate change-driven intracontinental range-expanding plants has been studied almost exclusively under controlled conditions, whereas little is known about actual patterns in the field. Here, we use novel molecular sequencing techniques combined with morphological quantification in order to examine nematode communities in the rhizospheres of four range-expanding and four congeneric native species along a 2,000 km latitudinal transect from South-Eastern to North-Western Europe. We tested the hypotheses that latitudinal shifts in nematode community composition are stronger in range-expanding plant species than in congeneric natives and that in their new range, range-expanding plant species accumulate fewest root-feeding nematodes. Our results show latitudinal variation in nematode community composition of both range expanders and native plant species, while operational taxonomic unit richness remained the same across ranges. Therefore, range-expanding plant species face different nematode communities at higher latitudes, but this is also the case for widespread native plant species. Only one of the four range-expanding plant species showed a stronger shift in nematode community composition than its congeneric native and accumulated fewer root-feeding nematodes in its new range. We conclude that variation in nematode community composition with increasing latitude occurs for both range-expanding and native plant species and that some range-expanding plant species may become released from root-feeding nematodes in the new range.
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Nematoides , Solo , Animais , Europa (Continente) , Plantas , RizosferaRESUMO
Current climate warming enables plant species and soil organisms to expand their range to higher latitudes and altitudes. At the same time, climate change increases the incidence of extreme weather events such as drought. While it is expected that plants and soil organisms originating from the south are better able to cope with drought, little is known about the consequences of their range shifts on soil functioning under drought events.Here, we test how range-expanding plant species and soil communities may influence soil functioning under drought. We performed a full-factorial outdoor mesocosm experiment with plant communities of range expanders or related natives, with soil inocula from the novel or the original range, with or without summer drought. We measured litter decomposition, carbon mineralization and enzyme activities, substrate-induced respiration and the relative abundance of soil saprophytic fungi immediately after drought and at 6 and 12 weeks after rewetting.Drought decreased all soil functions regardless of plant and soil origin except one; soil respiration was less reduced in soils of range-expanding plant communities, suggesting stronger resistance to drought. After rewetting, soil functioning responses depended on plant and soil origin. Soils of native plant communities with a history of drought had more litter mass loss and higher relative abundance of saprophytic fungi than soils without drought and soils of range expanders. Functions of soil from range expanders recovered in a more conservative manner than soils of natives, as litter mass loss did not exceed the control rates. At the end of the experiment, after rewetting, most soil functions in mesocosms with drought history did not differ anymore from the control.We conclude that functional consequences of range-expanding plants and soil biota may interact with effects of drought and that these effects are most prominent during the first weeks after rewetting of the soil. A free http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13453/suppinfo can be found within the Supporting Information of this article.
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Plant range expansion is occurring at a rapid pace, largely in response to human-induced climate warming. Although the movement of plants along latitudinal and altitudinal gradients is well-documented, effects on belowground microbial communities remain largely unknown. Furthermore, for range expansion, not all plant species are equal: in a new range, the relatedness between range-expanding plant species and native flora can influence plant-microorganism interactions. Here we use a latitudinal gradient spanning 3,000 km across Europe to examine bacterial and fungal communities in the rhizosphere and surrounding soils of range-expanding plant species. We selected range-expanding plants with and without congeneric native species in the new range and, as a control, the congeneric native species, totalling 382 plant individuals collected across Europe. In general, the status of a plant as a range-expanding plant was a weak predictor of the composition of bacterial and fungal communities. However, microbial communities of range-expanding plant species became more similar to each other further from their original range. Range-expanding plants that were unrelated to the native community also experienced a decrease in the ratio of plant pathogens to symbionts, giving weak support to the enemy release hypothesis. Even at a continental scale, the effects of plant range expansion on the belowground microbiome are detectable, although changes to specific taxa remain difficult to decipher.
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Microbiota , Plantas/microbiologia , Rizosfera , Bactérias/genética , Bactérias/isolamento & purificação , Mudança Climática , DNA Bacteriano/análise , DNA Fúngico/análise , Europa (Continente) , Fungos/genética , Fungos/isolamento & purificação , Microbiologia do SoloRESUMO
It is increasingly acknowledged that climate change is influencing terrestrial ecosystems by increased drought and rainfall intensities. Soil microbes are key drivers of many processes in terrestrial systems and rely on water in soil pores to fulfill their life cycles and functions. However, little is known on how drought and rainfall fluctuations, which affect the composition and structure of microbial communities, persist once original moisture conditions have been restored. Here, we study how simulated short-term drying and re-wetting events shape the community composition of soil fungi and prokaryotes. In a mesocosm experiment, soil was exposed to an extreme drought, then re-wetted to optimal moisture (50% WHC, water holding capacity) or to saturation level (100% WHC). Composition, community structure and diversity of microbes were measured by sequencing ITS and 16S rRNA gene amplicons 3 weeks after original moisture content had been restored. Drying and extreme re-wetting decreased richness of microbial communities, but not evenness. Abundance changes were observed in only 8% of prokaryote OTUs, and 25% of fungal OTUs, whereas all other OTUs did not differ between drying and re-wetting treatments. Two specific legacy response groups (LRGs) were observed for both prokaryotes and fungi. OTUs belonging to the first LRG decreased in relative abundance in soil with a history of drought, whereas OTUs that increased in soil with a history of drought formed a second LRG. These microbial responses were spread among different phyla. Drought appeared to be more important for the microbial community composition than the following extreme re-wetting. 16S profiles were correlated with both inorganic N concentration and basal respiration and ITS profiles correlated with fungal biomass. We conclude that a drying and/or an extreme re-wetting history can persist in soil microbial communities via specific response groups composed of members with broad phylogenetic origins, with possible functional consequences on soil processes and plant species. As a large fraction of OTUs responding to drying and re-wetting belonged to the rare biosphere, our results suggest that low abundant microbial species are potentially important for ecosystem responses to extreme weather events.
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Climate change is accelerating the spread of plants and their associated species to new ranges. The differences in range shift capacity of the various types of species may disrupt long-term co-evolved relationships especially those belowground, however, this may be less so for seed-borne endophytic microbes. We collected seeds and soil of the range-expanding Centaurea stoebe and the congeneric Centaurea jacea from three populations growing in Slovenia (native range of both Centaurea species) and the Netherlands (expanded range of C. stoebe, native range of C. jacea). We isolated and identified endophytic fungi directly from seeds, as well as from roots of the plants grown in Slovenian, Dutch or sterilized soil to compare fungal endophyte composition. Furthermore, we investigated whether C. stoebe hosts a reduced community composition of endophytes in the expanded range due to release from plant-species specific fungi while endophyte communities in C. jacea in both ranges are similar. We cultivated 46 unique and phylogenetically diverse endophytes. A majority of the seed endophytes resembled potential pathogens, while most root endophytes were not likely to be pathogenic. Only one endophyte was found in both roots and seeds, but was isolated from different plant species. Unexpectedly, seed endophyte diversity of southern C. stoebe populations was lower than of populations from the north, while the seed endophyte community composition of northern C. stoebe populations was significantly different southern C. stoebe as well as northern and southern C. jacea populations. Root endophyte diversity was considerably lower in C. stoebe than in C. jacea independent of plant and soil origin, but this difference disappeared when plants were grown in sterile soils. We conclude that the community composition of fungal endophytes not only differs between related plant species but also between populations of plants that expand their range compared to their native habitat. Our results suggest that fungal endophytes of two Centaurea species are not able to systemically infect plants. We highlight that endophytes remain poorly studied and further work should investigate the functional importance of endophytes.
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Plant-soil feedback (PSF) and plant competition play an important role in structuring vegetation composition, but their interaction remains unclear. Recent studies suggest that competing plants could dilute pathogenic effects, whereas the standing view is that competition may increase the sensitivity of the focal plant to PSF. In agro-ecosystems each of these two options would yield contrasting outcomes: reduced versus enhanced effects of weeds on crop biomass production. To test the effect of competition on sensitivity to PSF, we grew Triticum aestivum (Common wheat) with and without competition from a weed community composed of Vicia villosa, Chenopodium album and Myosotis arvensis. Plants were grown in sterilized soil, with or without living field inoculum from 4 farms in the UK. In the conditioning phase, field inocula had both positive and negative effects on T. aestivum shoot biomass, depending on farm. In the feedback phase the differences between shoot biomass in T. aestivum monoculture on non-inoculated and inoculated soils had mostly disappeared. However, T. aestivum plants growing in mixtures in the feedback phase were larger on non-inoculated soil than on inoculated soil. Hence, T. aestivum was more sensitive to competition when the field soil biota was present. This was supported by the statistically significant negative correlation between shoot biomass of weeds and T. aestivum, which was absent on sterilized soil. In conclusion, competition in cereal crop-weed systems appears to increase cereal crop sensitivity to soil biota.