Farming practices to enhance biodiversity across biomes: a systematic review.

Intensive agriculture for food and feed production is a key driver of global biodiversity loss. It is generally assumed that more extensive practices are needed to reconcile food production with biodiversity conservation. In a literature review across biomes and for seven taxa, we retrieved 35 alternative practices (e.g. no-tillage, cover crops, organic fertilizer) from 331 studies. We found that no single practice enhanced all taxonomic groups, but that overall less intensive agricultural practices are beneficial to biodiversity. Nevertheless, often practices had no effects observed and very rarely contrasting impacts on aboveground versus belowground taxa. Species responses to practices were mostly consistent across biomes, except for fertilization. We conclude that alternative practices generally enhance biodiversity, but there is also variation in impacts depending on taxonomic group or type of practice. This suggests that a careful selection of practices is needed to secure biodiversity across taxa in future food systems worldwide.

Normalized difference vegetation index analysis reveals increase of biomass production and stability during the conversion from conventional to organic farming.

Monitoring agriculture by remote sensing enables large-scale evaluation of biomass production across space and time. The normalized difference vegetation index (NDVI) is used as a proxy for green biomass. Here, we used satellite-derived NDVI of arable farms in the Netherlands to evaluate changes in biomass following conversion from conventional to organic farming. We compared NDVI and the stability of NDVI across 72 fields on sand and marine clay soils. Thirty-six of these fields had been converted into organic agriculture between 0 and 50 years ago (with 2017 as reference year), while the other 36 were paired control fields where conventional farming continued. We used high-resolution images from the Sentinel-2 satellite to obtain NDVI estimates across 5 years (January 2016-October 2020). Overall, NDVI did not differ between conventional and organic management during the time series, but NDVI stability was significantly higher under organic management. NDVI was lower under organic management in sandy, but not in clay, soils. Organic farms that had been converted less than ~19 years ago had lower NDVI than conventional farms. However, the difference diminished over time and eventually turned positive after ~19 years since the conversion. NDVI, averaged across the 5 years of study, was positively correlated to soil Olsen-P measured from soil samples collected in 2017. We conclude that NDVI in organic fields was more stable than in conventional fields, and that the lower biomass in the early years since the transition to organic agriculture can be overcome with time. Our study also indicates the role of soil P bioavailability for plant biomass production across the examined fields, and the benefit of combining remote sensing with on-site soil measurements to develop a more mechanistic understanding that may help us navigate the transition to a more sustainable type of agriculture.

High-resolution methylome analysis uncovers stress-responsive genomic hotspots and drought-sensitive transposable element superfamilies in the clonal Lombardy poplar.

DNA methylation is environment-sensitive and can mediate stress responses. In trees, changes in the environment might cumulatively shape the methylome landscape over time. However, because high-resolution methylome studies usually focus on single environmental cues, the stress-specificity and long-term stability of methylation responses remain unclear. Here, we studied the methylome plasticity of a Populus nigra cv. 'Italica' clone widely distributed across Europe. Adult trees from different geographic locations were clonally propagated in a common garden experiment and exposed to cold, heat, drought, herbivory, rust infection, and salicylic acid treatments. Whole-genome bisulfite sequencing revealed stress-induced and naturally occurring DNA methylation variants. In CG/CHG contexts, the same genomic regions were often affected by multiple stresses, suggesting a generic methylome response. Moreover, these variants showed striking overlap with naturally occurring methylation variants between trees from different locations. Drought treatment triggered CHH hypermethylation of transposable elements, affecting entire superfamilies near drought-responsive genes. Thus, we revealed genomic hotspots of methylation change that are not stress-specific and that contribute to natural DNA methylation variation, and identified stress-specific hypermethylation of entire transposon superfamilies with possible functional consequences. Our results underscore the importance of studying multiple stressors in a single experiment for recognizing general versus stress-specific methylome responses.

Plant-soil interactions during the native and exotic range expansion of an annual plant.

Range expansions, whether they are biological invasions or climate change-mediated range shifts, may have profound ecological and evolutionary consequences for plant-soil interactions. Range-expanding plants encounter soil biota with which they have a limited coevolutionary history, especially when introduced to a new continent. Past studies have found mixed results on whether plants experience positive or negative soil feedback interactions in their novel range, and these effects often change over time. One important theoretical explanation is that plants locally adapt to the soil pathogens and mutualists in their novel range. We tested this hypothesis in Dittrichia graveolens, an annual plant that is both expanding its European native range, initially coinciding with climate warming, and rapidly invading California after human introduction. In parallel greenhouse experiments on both continents, we used plant genotypes and soils from 5 locations at the core and edge of each range to compare plant growth in soil inhabited by D. graveolens and nearby control microsites as a measure of plant-soil feedback. Plant-soil interactions were highly idiosyncratic across each range. On average, plant-soil feedbacks were more positive in the native range than in the exotic range. In line with the strongly heterogeneous pattern of soil responses along our biogeographic gradients, we found no evidence for evolutionary differentiation between plant genotypes from the core to the edge of either range. Our results suggest that the evolution of plant-soil interactions during range expansion may be more strongly driven by local evolutionary dynamics varying across the range than by large-scale biogeographic shifts.

Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome.

BACKGROUND: Soil microbiomes are increasingly acknowledged to affect plant functioning. Research in molecular model species Arabidopsis thaliana has given detailed insights of such plant-microbiome interactions. However, the circumstances under which natural A. thaliana plants have been studied so far might represent only a subset of A. thaliana's full ecological context and potential biotic diversity of its root-associated microbiome. RESULTS: We collected A. thaliana root-associated soils from a secondary succession gradient covering 40 years of land abandonment. All field sites were situated on the same parent soil material and in the same climatic region. By sequencing the bacterial and fungal communities and soil abiotic analysis we discovered differences in both the biotic and abiotic composition of the root-associated soil of A. thaliana and these differences are in accordance with the successional class of the field sites. As the studied sites all have been under (former) agricultural use, and a climatic cline is absent, we were able to reveal a more complete variety of ecological contexts A. thaliana can appear and sustain in. CONCLUSIONS: Our findings lead to the conclusion that although A. thaliana is considered a pioneer plant species and previously almost exclusively studied in early succession and disturbed sites, plants can successfully establish in soils which have experienced years of ecological development. Thereby, A. thaliana can be exposed to a much wider variation in soil ecological context than is currently presumed. This knowledge opens up new opportunities to enhance our understanding of causal plant-microbiome interactions as A. thaliana cannot only grow in contrasting soil biotic and abiotic conditions along a latitudinal gradient, but also when those conditions vary along a secondary succession gradient. Future research could give insights in important plant factors to grow in more ecologically complex later-secondary succession soils, which is an impending direction of our current agricultural systems.

Linking above and belowground carbon sequestration, soil organic matter properties, and soil health in Brazilian Atlantic Forest restoration.

Forest restoration mitigates climate change by removing CO2 and storing C in terrestrial ecosystems. However, incomplete information on C storage in restored tropical forests often fails to capture the ecosystem's holistic C dynamics. This study provides an integrated assessment of C storage in above to belowground subsystems, its consequences for greenhouse gas (GHG) fluxes, and the quantity, quality, and origin of soil organic matter (SOM) in restored Atlantic forests in Brazil. Relations between SOM properties and soil health indicators were also explored. We examined two restorations using tree planting ('active restoration'): an 8-year-old forest with green manure and native trees planted in two rounds, and a 15-year-old forest with native-planted trees in one round without green manure. Restorations were compared to reformed pasture and primary forest sites. We measured C storage in soil layers (0-10, 10-20, and 20-30 cm), litter, and plants. GHG emissions were assessed using CH4 and CO2 fluxes. SOM quantity was evaluated using C and N, quality using humification index (HLIFS), and origin using δ13C and δ15N. Nine soil health indicators were interrelated with SOM attributes. The primary forest presented the highest C stocks (107.7 Mg C ha-1), followed by 15- and 8-year-old restorations and pasture with 69.8, 55.5, and 41.8 Mg C ha-1, respectively. Soil C stocks from restorations and pasture were 20% lower than primary forest. However, 8- and 15-year-old restorations stored 12.3 and 28.3 Mg ha-1 more aboveground C than pasture. The younger forest had δ13C and δ15N values of 2.1 and 1.7‰, respectively, lower than the 15-year-old forest, indicating more C derived from C3 plants and biological N fixation. Both restorations and pasture had at least 34% higher HLIFS in deeper soil layers (10-30 cm) than primary forest, indicating a lack of labile SOM. Native and 15-year-old forests exhibited higher soil methane influx (141.1 and 61.9 µg m-2 h-1). Forests outperformed pasture in most soil health indicators, with 69% of their variance explained by SOM properties. However, SOM quantity and quality regeneration in both restorations approached the pristine forest state only in the top 10 cm layer, while deeper soil retained agricultural degradation legacies. In conclusion, active restoration of the Atlantic Forest is a superior approach compared to pasture reform for GHG mitigation. Nonetheless, the development of restoration techniques to facilitate labile C input into deeper soil layers (>10 cm) is needed to further improve soil multifunctionality and long-term C storage.

Forest restoration rehabilitates soil multifunctionality in riparian zones of sugarcane production landscapes.

Brazilian sugarcane plays a vital role in the production of both sugar and renewable energy. However, land use change and long-term conventional sugarcane cultivation have degraded entire watersheds, including a substantial loss of soil multifunctionality. In our study, riparian zones have been reforested to mitigate these impacts, protect aquatic ecosystems, and restore ecological corridors within the sugarcane production landscapes. We examined (i) how forest restoration enables rehabilitation of the soil's multifunctionality after long-term sugarcane cultivation and (ii) how long it takes to regain ecosystem functions comparable to those of a primary forest. We investigated a time series of riparian forests at 6, 15, and 30 years after starting restoration by planting trees (named 'active restoration') and determined soil C stocks, δ13C (indicative of C origin), as well as measures indicative of soil health. A primary forest and a long-term sugarcane field were used as references. Eleven soil physical, chemical, and biological indicators were used for a structured soil health assessment, calculating index scores based on soil functions. Forest-to-cane conversion reduced 30.6 Mg ha-1 of soil C stocks, causing soil compaction and loss of cation exchange capacity, thus degrading soil's physical, chemical, and biological functions. Forest restoration for 6-30 years recovered 16-20 Mg C ha-1 stored in soils. In all restored sites, soil functions such as supporting root growth, aerating the soil, nutrient storage capacity, and providing C energy for microbial activity were gradually recovered. Thirty years of active restoration was sufficient to reach the primary forest state in overall soil health index, multifunctional performance, and C sequestration. We conclude that active forest restoration in sugarcane-dominated landscapes is an effective way to restore soil multifunctionality approaching the level of the native forest in approximately three decades. Moreover, the C sequestration in the restored forest soils will help to mediate global warming.

Mycorrhiza-mediated recruitment of complete denitrifying Pseudomonas reduces N2O emissions from soil.

BACKGROUND: Arbuscular mycorrhizal fungi (AMF) are key soil organisms and their extensive hyphae create a unique hyphosphere associated with microbes actively involved in N cycling. However, the underlying mechanisms how AMF and hyphae-associated microbes may cooperate to influence N2O emissions from "hot spot" residue patches remain unclear. Here we explored the key microbes in the hyphosphere involved in N2O production and consumption using amplicon and shotgun metagenomic sequencing. Chemotaxis, growth and N2O emissions of isolated N2O-reducing bacteria in response to hyphal exudates were tested using in vitro cultures and inoculation experiments. RESULTS: AMF hyphae reduced denitrification-derived N2O emission (max. 63%) in C- and N-rich residue patches. AMF consistently enhanced the abundance and expression of clade I nosZ gene, and inconsistently increased that of nirS and nirK genes. The reduction of N2O emissions in the hyphosphere was linked to N2O-reducing Pseudomonas specifically enriched by AMF, concurring with the increase in the relative abundance of the key genes involved in bacterial citrate cycle. Phenotypic characterization of the isolated complete denitrifying P. fluorescens strain JL1 (possessing clade I nosZ) indicated that the decline of net N2O emission was a result of upregulated nosZ expression in P. fluorescens following hyphal exudation (e.g. carboxylates). These findings were further validated by re-inoculating sterilized residue patches with P. fluorescens and by an 11-year-long field experiment showing significant positive correlation between hyphal length density with the abundance of clade I nosZ gene. CONCLUSIONS: The cooperation between AMF and the N2O-reducing Pseudomonas residing on hyphae significantly reduce N2O emissions in the microsites. Carboxylates exuded by hyphae act as attractants in recruiting P. fluorescens and also as stimulants triggering nosZ gene expression. Our discovery indicates that reinforcing synergies between AMF and hyphosphere microbiome may provide unexplored opportunities to stimulate N2O consumption in nutrient-enriched microsites, and consequently reduce N2O emissions from soils. This knowledge opens novel avenues to exploit cross-kingdom microbial interactions for sustainable agriculture and for climate change mitigation. Video Abstract.

Soil biodiversity needs policy without borders.

Soil health laws should account for global soil connections.

Soil legacy effects of plants and drought on aboveground insects in native and range-expanding plant communities.

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.

Soil aggregate microbiomes steer plant community overyielding in ungrazed and intensively grazed grassland soils.

Plant and soil microbial community composition play a central role in maintaining ecosystem functioning. Most studies have focused on soil microbes in the bulk soil, the rhizosphere and inside plant roots, however, less is known about the soil community that exists within soil aggregates, and how these soil communities influence plant biomass production. Here, using field-conditioned soil collected from experimental ungrazed and grazed grasslands in Inner Mongolia, China, we examined the composition of microbiomes inside soil aggregates of various size classes, and determined their roles in plant-soil feedbacks (PSFs), diversity-productivity relationships, and diversity-dependent overyielding. We found that grazing induced significantly positive PSF effects, which appeared to be mediated by mycorrhizal fungi, particularly under plant monocultures. Despite this, non-additive effects of microbiomes within different soil aggregates enhanced the strength of PSF under ungrazed grassland, but decreased PSF strength under intensively grazed grassland. Plant mixture-related increases in PSF effects markedly enhanced diversity-dependent overyielding, primarily due to complementary effects. Selection effects played far less of a role. Our work suggests that PSF contributes to diversity-dependent overyielding in grasslands via non-additive effects of microbiomes within different soil aggregates. The implication of our work is that assessing the effectiveness of sustainable grassland restoration and management on soil properties requires inspection of soil aggregate size-specific microbiomes, as these are relevant determinants of the feedback interactions between soil and plant performance.

Biotic responses to climate extremes in terrestrial ecosystems.

Anthropogenic climate change is increasing the incidence of climate extremes. Consequences of climate extremes on biodiversity can be highly detrimental, yet few studies also suggest beneficial effects of climate extremes on certain organisms. To obtain a general understanding of ecological responses to climate extremes, we present a review of how 16 major taxonomic/functional groups (including microorganisms, plants, invertebrates, and vertebrates) respond during extreme drought, precipitation, and temperature. Most taxonomic/functional groups respond negatively to extreme events, whereas groups such as mosses, legumes, trees, and vertebrate predators respond most negatively to climate extremes. We further highlight that ecological recovery after climate extremes is challenging to predict purely based on ecological responses during or immediately after climate extremes. By accounting for the characteristics of the recovering species, resource availability, and species interactions with neighboring competitors or facilitators, mutualists, and enemies, we outline a conceptual framework to better predict ecological recovery in terrestrial ecosystems.

Soil microbial diversity and community composition during conversion from conventional to organic agriculture.

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.

Effects of Light Quality on Colonization of Tomato Roots by AMF and Implications for Growth and Defense.

Beneficial soil microbes can enhance plant growth and defense, but the extent to which this occurs depends on the availability of resources, such as water and nutrients. However, relatively little is known about the role of light quality, which is altered during shading, resulting a low red: far-red ratio (R:FR) of light. We examined how low R:FR light influences arbuscular mycorrhizal fungus (AMF)-mediated changes in plant growth and defense using Solanum lycopersicum (tomato) and the insect herbivore Chrysodeixis chalcites. We also examined effects on third trophic level interactions with the parasitoid Cotesia marginiventris. Under low R:FR light, non-mycorrhizal plants activated the shade avoidance syndrome (SAS), resulting in enhanced biomass production. However, mycorrhizal inoculation decreased stem elongation in shaded plants, thus counteracting the plant's SAS response to shading. Unexpectedly, activation of SAS under low R:FR light did not increase plant susceptibility to the herbivore in either non-mycorrhizal or mycorrhizal plants. AMF did not significantly affect survival or growth of caterpillars and parasitoids but suppressed herbivore-induced expression of jasmonic acid-signaled defenses genes under low R:FR light. These results highlight the context-dependency of AMF effects on plant growth and defense and the potentially adverse effects of AMF under shading.

Temporal dynamics of range expander and congeneric native plant responses during and after extreme drought events.

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.

Microbial storage and its implications for soil ecology.

Organisms throughout the tree of life accumulate chemical resources, in particular forms or compartments, to secure their availability for future use. Here we review microbial storage and its ecological significance by assembling several rich but disconnected lines of research in microbiology, biogeochemistry, and the ecology of macroscopic organisms. Evidence is drawn from various systems, but we pay particular attention to soils, where microorganisms play crucial roles in global element cycles. An assembly of genus-level data demonstrates the likely prevalence of storage traits in soil. We provide a theoretical basis for microbial storage ecology by distinguishing a spectrum of storage strategies ranging from surplus storage (storage of abundant resources that are not immediately required) to reserve storage (storage of limited resources at the cost of other metabolic functions). This distinction highlights that microorganisms can invest in storage at times of surplus and under conditions of scarcity. We then align storage with trait-based microbial life-history strategies, leading to the hypothesis that ruderal species, which are adapted to disturbance, rely less on storage than microorganisms adapted to stress or high competition. We explore the implications of storage for soil biogeochemistry, microbial biomass, and element transformations and present a process-based model of intracellular carbon storage. Our model indicates that storage can mitigate against stoichiometric imbalances, thereby enhancing biomass growth and resource-use efficiency in the face of unbalanced resources. Given the central roles of microbes in biogeochemical cycles, we propose that microbial storage may be influential on macroscopic scales, from carbon cycling to ecosystem stability.

Global data on earthworm abundance, biomass, diversity and corresponding environmental properties.

Earthworms are an important soil taxon as ecosystem engineers, providing a variety of crucial ecosystem functions and services. Little is known about their diversity and distribution at large spatial scales, despite the availability of considerable amounts of local-scale data. Earthworm diversity data, obtained from the primary literature or provided directly by authors, were collated with information on site locations, including coordinates, habitat cover, and soil properties. Datasets were required, at a minimum, to include abundance or biomass of earthworms at a site. Where possible, site-level species lists were included, as well as the abundance and biomass of individual species and ecological groups. This global dataset contains 10,840 sites, with 184 species, from 60 countries and all continents except Antarctica. The data were obtained from 182 published articles, published between 1973 and 2017, and 17 unpublished datasets. Amalgamating data into a single global database will assist researchers in investigating and answering a wide variety of pressing questions, for example, jointly assessing aboveground and belowground biodiversity distributions and drivers of biodiversity change.

Plant-Soil Feedbacks and Temporal Dynamics of Plant Diversity-Productivity Relationships.

Plant-soil feedback (PSF) and diversity-productivity relationships are important research fields to study drivers and consequences of changes in plant biodiversity. While studies suggest that positive plant diversity-productivity relationships can be explained by variation in PSF in diverse plant communities, key questions on their temporal relationships remain. Here, we discuss three processes that change PSF over time in diverse plant communities, and their effects on temporal dynamics of diversity-productivity relationships: spatial redistribution and changes in dominance of plant species; phenotypic shifts in plant traits; and dilution of soil pathogens and increase in soil mutualists. Disentangling these processes in plant diversity experiments will yield new insights into how plant diversity-productivity relationships change over time.

Globally, plant-soil feedbacks are weak predictors of plant abundance.

Plant-soil feedbacks (PSFs) have been shown to strongly affect plant performance under controlled conditions, and PSFs are thought to have far reaching consequences for plant population dynamics and the structuring of plant communities. However, thus far the relationship between PSF and plant species abundance in the field is not consistent. Here, we synthesize PSF experiments from tropical forests to semiarid grasslands, and test for a positive relationship between plant abundance in the field and PSFs estimated from controlled bioassays. We meta-analyzed results from 22 PSF experiments and found an overall positive correlation (0.12 ≤  r ¯  ≤ 0.32) between plant abundance in the field and PSFs across plant functional types (herbaceous and woody plants) but also variation by plant functional type. Thus, our analysis provides quantitative support that plant abundance has a general albeit weak positive relationship with PSFs across ecosystems. Overall, our results suggest that harmful soil biota tend to accumulate around and disproportionately impact species that are rare. However, data for the herbaceous species, which are most common in the literature, had no significant abundance-PSFs relationship. Therefore, we conclude that further work is needed within and across biomes, succession stages and plant types, both under controlled and field conditions, while separating PSF effects from other drivers (e.g., herbivory, competition, disturbance) of plant abundance to tease apart the role of soil biota in causing patterns of plant rarity versus commonness.