Management effects on soil nematode abundance differ among functional groups and land-use types at a global scale.

Anthropogenic land use is threatening global biodiversity. As one of the most abundant animals on Earth, nematodes occupy several key positions in belowground food webs and contribute to many ecosystem functions and services. However, the effects of land use on nematode abundance and its determinants remain poorly understood at a global scale. To characterize nematodes' responses to land use across trophic groups, we used a dataset of 6,825 soil samples globally to assess how nematode abundance varies among regional land-use types (i.e. primary vegetation, secondary vegetation, pasture, cropland and urban) and local land-use intensities (i.e. human-managed or not). We also quantified the interactive effects of land use and environmental predictors (i.e. mean annual temperature, annual precipitation, soil organic carbon, soil pH, global vegetation biomass and global vegetation productivity) on nematode abundance. We found that total nematode abundance and the abundance of bacterivores, fungivores, herbivores, omnivores and predators generally increased or were not affected under management across land-use types. Specifically, the most numerically abundant bacterivores were higher in managed than in unmanaged secondary vegetation habitats and urban areas, and herbivores were more abundant in managed than in unmanaged primary and secondary vegetation habitats. Furthermore, the numbers of significant environmental predictors of nematode abundance were reduced and the magnitude and the direction of the predictors were changed under management. We also found that nematode abundance was more variable and less determined by environmental factors in urban than in other land-use types. These findings challenge the view that human land use decreases animal abundance across trophic groups, but highlight that land use is altering the trophic composition of soil nematodes and its relationships with the environment at the global scale.

Spatial patterns and ecological drivers of soil nematode ß-diversity in natural grasslands vary among vegetation types and trophic position.

Understanding biogeographic patterns of community assemblages is a core objective in ecology, but for soil communities these patterns are poorly understood. To understand the spatial patterns and underlying mechanisms of ß-diversity in soil communities, we investigated the ß-diversity of soil nematode communities along a 3,200-km transect across semi-arid and arid grasslands. Spatial turnover and nested-resultant are the two fundamental components of ß-diversity, which have been attributed to various processes of community assembly. We calculated the spatial turnover and nested-resultant components of soil nematode ß-diversity based on the ß-partitioning framework. Distance matrices for the dissimilarity of soil nematode communities were computed using the 'Sørensen' method. We fitted negative exponential models to compare the distance decay patterns in nematode community similarity with geographic distance and plant community distance in three vegetation types (desert, desert steppe and typical steppe) and along the whole transect. Variation partitioning was used to distinguish the contribution of geographic distance and environmental variables to ß-diversity and the partitioned components. Geographic distance and environmental filtering jointly drove the ß-diversity patterns of nematode community, but environmental filtering explained more of the variation in ß-diversity in the desert and typical steppe, whereas geographic distance was important in the desert steppe. Nematode community assembly was explained more by the spatial turnover component than by the nested-resultant component. For nematode feeding groups, the ß-diversity in different vegetation types increased with geographic distance and plant community distance, but the nested-resultant component of bacterial feeders in the desert ecosystem decreased with geographic distance and plant community distance. Our findings show that spatial variation in soil nematode communities is regulated by environmental processes at the vegetation type scale, while spatial processes mainly work on the regional scale, and emphasize that the spatial patterns and drivers of nematode ß-diversity differ among trophic levels. Our study provides insight into the ecological processes that maintain soil biodiversity and biogeographic patterns of soil community assemblage at large spatial scales.

Next-generation sequencing of the soil nematode community enables the sustainability of banana plantations to be monitored.

Uganda faces a considerable challenge to match its food production to an annual population growth rate of 3%. Cooking bananas are the country's most produced staple crop but the annual national harvest is not increasing. The crop grows on infertile soils that are normally fertilised organically and often susceptible to erosion. Soil nematodes are well-established as bioindicators of soil quality that can support environmental monitoring and assessment of the sustainability of agricultural systems. These invertebrates are a highly ranked indicator of biodiversity with molecular approaches available. Consequently, we have applied next-generation DNA sequencing of soil nematodes to evaluate soil quality of Ugandan banana plantations. The aim is to establish a method for constructing an aspect of an environmental biosafety dossier with the future aim of assessing the impact of transgenic crops and improving current cropping systems. The soil samples did not differ significantly in any of the measured soil chemistry factors, soil texture or percentage of organic matter. Thirty taxons of soil nematodes other than the plant parasites were recovered from soil supporting nine banana plantations plus three each from coffee and banana-coffee interplants from East and West Uganda. Cluster analysis correctly allocated each plantation to the crop/intercrop being grown when based on the abundance of taxa rather than taxa presence or absence. This indicates that the host has considerable effects on the abundance of specific nematode species within the soil. Overall, nematodes were more abundant in soil from coffee plantations than from banana-coffee interplants with the lowest values being from fields supporting just banana. Only the basal and trophic diversity indices and the percentage of nematodes that are rapid colonisers varied between the three plantation types. The soil of all fifteen plantations can be classified as having a mature soil web condition with low physical disturbance, limited chemical stressors, moderately high nutrient enrichment and balanced decomposition channels.

Differential biodiversity responses between kingdoms (plants, fungi, bacteria and metazoa) along an Alpine succession gradient.

Biological diversities of multiple kingdoms potentially respond in similar ways to environmental changes. However, studies either compare details of microbial diversity across general vegetation or land use classes or relate details of plant community diversity with the extent of microbially governed soil processes, via physiological profiling. Here, we test the hypothesis of shared responses of plant and rhizosphere bacterial, fungal and metazoan biodiversities (especially across-habitat ß-diversity patterns) along a disturbance gradient encompassing grazed to abandoned Alpine pasture, on acid soil in the European Central Alps. Rhizosphere biological diversity was inferred from eDNA fractions specific to bacteria, fungi and metazoans from contrasting plant habitats indicative of different disturbance levels. We found that soil ß-diversity patterns were weakly correlated with plant diversity measures and similarly ordinated along an evident edaphic (pH, C:N, assimilable P) and disturbance gradient but, contrary to our hypothesis, did not demonstrate the same diversity patterns. While plant communities were well separated along the disturbance gradient, correlating with fungal diversity, the majority of bacterial taxa were shared between disturbance levels (75% of bacteria were ubiquitous, cf. 29% plant species). Metazoa exhibited an intermediate response, with communities at the lowest levels of disturbance partially overlapping. Thus, plant and soil biological diversities were only loosely dependent and did not exhibit strictly linked environmental responses. This probably reflects the different spatial scales of organisms (and their habitats) and capacity to invest resources in persistent multicellular tissues, suggesting that vegetation responses to environmental change are unreliable indicators of below-ground biodiversity responses.

Using metagenomics to show the efficacy of forest restoration in the New Jersey Pine Barrens.

The Franklin Parker Preserve within the New Jersey Pine Barrens contains 5000 acres of wetlands habitat, including old-growth Atlantic white cedar (or AWC; Chamaecyparis thyoides) swamps, cranberry bogs, and former cranberry bogs undergoing restoration into AWC forests. This study showed that the C-use efficiency was greater in the old-growth AWC soils than in soils from 8-year-old mid-stage restored AWC stands, which were greater than found in soil from 4-year-old AWC stands-the latter two stands being restored from long-term cranberry bogs. A metagenomic analysis of eDNA extracted from these soils showed that the C-cycle trends were associated with increases in the relative numbers of DNA sequences from several copiotrophic bacterial groups (Bacteroidetes and Proteobacteria), complex C-decomposing fungal groups (Sordiomycetes, Mortierellales, and Thelephorales), and collembolan and formicid invertebrates. All groups are indicators of successionally more advanced soils, and critical for soil C-cycle activities. These data suggest that the restoration activities studied are enhancing critical guilds of soil biota, and increasing C-use efficiency in the soils of restored habitats, and that the use of metagenomic analysis of soil eDNA can be used in the development of assessment models for soil recovery of wetlands following restoration.

Bacterial Community Diversity in Soil Under two Tillage Practices as Determined by Pyrosequencing.

The ability of soil to provide ecosystem services is dependent on microbial diversity, with 80-90 % of the processes in soil being mediated by microbes. There still exists a knowledge gap in the types of microorganisms present in soil and how soil management affects them. However, identification of microorganisms is severely limited by classical culturing techniques that have been traditionally used in laboratories. Metagenomic approaches are increasingly becoming common, with current high-throughput sequencing approaches allowing for more in-depth analysis. We conducted a preliminary analysis of bacterial diversity in soils from the longest continuously maintained no-till (NT) plots in the world (52 years) and in adjacent plow-till (PT) plots in Ohio, USA managed similarly except for tillage. Bacterial diversity was determined using a culture-independent approach of high-throughput pyrosequencing of the 16S rRNA gene. Proteobacteria and Acidobacteria were predominant in both samples but the NT soil had a higher number of reads, bacterial richness, and five unique phyla. Four unique phyla were observed in PT and 99 % of the community had relative abundance of <1 %. Plowing and secondary tillage tend to homogenize the soil and reduces the unique (i.e., diverse) microenvironments where microbial populations can reside. We conclude that tillage leads to fewer dominant species being present in soil and that these species contribute to a higher percentage of the total community.

Oomycete Soil Diversity Associated with Betula and Alnus in Forests and Urban Settings in the Nordic-Baltic Region.

This study aimed to determine the differences and drivers of oomycete diversity and community composition in alder- and birch-dominated park and natural forest soils of the Fennoscandian and Baltic countries of Estonia, Finland, Lithuania, Norway, and Sweden. For this, we sequenced libraries of PCR products generated from the DNA of 111 soil samples collected across a climate gradient using oomycete-specific primers on a PacBio high-throughput sequencing platform. We found that oomycete communities are most affected by temperature seasonality, annual mean temperature, and mean temperature of the warmest quarter. Differences in composition were partly explained by the higher diversity of Saprolegniales in Sweden and Norway, as both total oomycete and Saprolegniales richness decreased significantly at higher longitudes, potentially indicating the preference of this group of oomycetes for a more temperate maritime climate. None of the evaluated climatic variables significantly affected the richness of Pythiales or Peronosporales. Interestingly, the relative abundance and richness of Pythiales was higher at urban sites compared to forest sites, whereas the opposite was true for Saprolegniales. Additionally, this is the first report of Phytophthora gallica and P. plurivora in Estonia. Our results indicate that the composition of oomycetes in soils is strongly influenced by climatic factors, and, therefore, changes in climate conditions associated with global warming may have the potential to significantly alter the distribution range of these microbes, which comprise many important pathogens of plants.

Short-term plant-soil feedback experiment fails to predict outcome of competition observed in long-term field experiment.

Mounting evidence suggests that plant-soil feedbacks (PSF) may determine plant community structure. However, we still have a poor understanding of how predictions from short-term PSF experiments compare with outcomes of long-term field experiments involving competing plants. We conducted a reciprocal greenhouse experiment to examine how the growth of prairie grass species depended on the soil communities cultured by conspecific or heterospecific plant species in the field. The source soil came from monocultures in a long-term competition experiment (LTCE; Cedar Creek Ecosystem Science Reserve, MN, USA). Within the LTCE, six species of perennial prairie grasses were grown in monocultures or in eight pairwise competition plots for 12 years under conditions of low or high soil nitrogen availability. In six cases, one species clearly excluded the other; in two cases, the pair appeared to coexist. In year 15, we gathered soil from all 12 soil types (monocultures of six species by two nitrogen levels) and grew seedlings of all six species in each soil type for 7 weeks. Using biomass estimates from this greenhouse experiment, we predicted coexistence or competitive exclusion using pairwise PSFs, as derived by Bever and colleagues, and compared model predictions to observed outcomes within the LTCE. Pairwise PSFs among the species pairs ranged from negative, which is predicted to promote coexistence, to positive, which is predicted to promote competitive exclusion. However, these short-term PSF predictions bore no systematic resemblance to the actual outcomes of competition observed in the LTCE. Other forces may have more strongly influenced the competitive interactions or critical assumptions that underlie the PSF predictions may not have been met. Importantly, the pairwise PSF score derived by Bever et al. is only valid when the two species exhibit an internal equilibrium, corresponding to the Lotka-Volterra competition outcomes of stable coexistence and founder control. Predicting the other two scenarios, competitive exclusion by either species irrespective of initial conditions, requires measuring biomass in uncultured soil, which is methodologically challenging. Subject to several caveats that we discuss, our results call into question whether long-term competitive outcomes in the field can be predicted from the results of short-term PSF experiments.

Plant-soil feedback from eastern redcedar (Juniperus virginiana) inhibits the growth of grasses in encroaching range.

The encroachment of woody plants into grasslands is an ongoing global problem that is largely attributed to anthropogenic factors such as climate change and land management practices. Determining the mechanisms that drive successful encroachment is a critical step towards planning restoration and long-term management strategies. Feedbacks between soil and aboveground communities can have a large influence on the fitness of plants and must be considered as potentially important drivers for woody encroachment. We conducted a plant-soil feedback experiment in a greenhouse between eastern redcedar Juniperus virginiana and four common North American prairie grass species. We assessed how soils that had been occupied by redcedar, a pervasive woody encroacher in the Great Plains of North America, affected the growth of Andropogon gerardi, Schizachyrium scoparium, Bromus inermis, and Pascopyrum smithii over time. We evaluated the effect of redcedar on grass performance by comparing the height and biomass of individuals that were grown in live or sterilized conspecific or redcedar soil. We found redcedar created a negative plant-soil feedback that limited the growth of the cool season grasses B. inermis and P. smithii, reducing their overall biomass by >60%. These effects were found in both live and sterilized redcedar soils. In live soils, some growth suppression can be attributed to the negative effects of soil microbes. The limitation of grass growth in sterile soils indicates redcedar may exude an allelochemical into the soil that limits grass growth. Our results demonstrate that plant-soil feedback created by redcedar inhibits the growth of certain grass species. By creating a plant-plant interaction that negatively affects competitors, redcedars increase the probability of seedling survival until they can grow to overtop their neighbors. These results indicate plant-soil feedback is a mechanism of native woody plant encroachment which could be important in many systems yet is understudied.

Diversity and asynchrony in soil microbial communities stabilizes ecosystem functioning.

Theoretical and empirical advances have revealed the importance of biodiversity for stabilizing ecosystem functions through time. Despite the global degradation of soils, whether the loss of soil microbial diversity can destabilize ecosystem functioning is poorly understood. Here, we experimentally quantified the contribution of soil fungal and bacterial communities to the temporal stability of four key ecosystem functions related to biogeochemical cycling. Microbial diversity enhanced the temporal stability of all ecosystem functions and this pattern was particularly strong in plant-soil mesocosms with reduced microbial richness where over 50% of microbial taxa were lost. The stabilizing effect of soil biodiversity was linked to asynchrony among microbial taxa whereby different soil fungi and bacteria promoted different ecosystem functions at different times. Our results emphasize the need to conserve soil biodiversity for the provisioning of multiple ecosystem functions that soils provide to the society.

Plant-Soil Feedbacks for the Restoration of Degraded Mine Lands: A Review.

Much effort has been made to remediate the degraded mine lands that bring severe impacts to the natural environments. However, it remains unclear what drives the recovery of biodiversity and ecosystem functions, making the restoration of these fragile ecosystems a big challenge. The interactions among plant species, soil communities, and abiotic conditions, i.e., plant-soil feedbacks (PSFs), significantly influence vegetation development, plant community structure, and ultimately regulate the recovery of ecosystem multi-functionality. Here, we present a conceptual framework concerning PSFs patterns and potential mechanisms in degraded mine lands. Different from healthy ecosystems, mine lands are generally featured with harsh physical and chemical properties, which may have different PSFs and should be considered during the restoration. Usually, pioneer plants colonized in the mine lands can adapt to the stressful environment by forming tolerant functional traits and gathering specific soil microbial communities. Understanding the mechanisms of PSFs would enhance our ability to predict and alter both the composition of above- and below-ground communities, and improve the recovery of ecosystem functions in degraded mine lands. Finally, we put forward some challenges of the current PSFs study and discuss avenues for further research in the ecological restoration of degraded mine lands.

Impact of Dietary Protein Content on Soil Bacterial and Fungal Communities in a Rice-Crab Co-culture System.

Although co-culture of paddy fields with aquatic animals is lucrative, the ecological impacts of high-protein content entering the agricultural soil via animal pellet feed and feces have not been well studied. Moreover, the effects of dietary protein on soils and soil microbes remain unclear. To elucidate this, we examined soil bacterial and fungal community composition and temporal changes in paddy fields subjected to different protein-content diets via 16S/18S rRNA gene amplicon sequencing analysis with a high-throughput next-generation sequencer. MiSeq sequencing revealed that protein content significantly impacted fungal community structure. High-protein diets reduced bacterial community diversity and relative abundance in both July and October. The phylum-level bacterial taxonomic composition was not affected by diet treatment, while in fungi, a major phylum-level shift was evident. Hierarchically clustered analysis showed that high-protein diets significantly reduced the relative abundance of Brevundimonas in both July and October. Saprotrophic macrofungal diversity was negatively related to dietary protein content. Considering microbial community structure and environmental factors, ca. 15% protein content is appropriate for the rice-crab co-culture system that we studied.

In-Field Habitat Management to Optimize Pest Control of Novel Soil Communities in Agroecosystems.

The challenge of managing agroecosystems on a landscape scale and the novel structure of soil communities in agroecosystems both provide reason to focus on in-field management practices, including cover crop adoption, reduced tillage, and judicial pesticide use, to promote soil community diversity. Belowground and epigeal arthropods, especially exotic generalist predators, play a significant role in controlling insect pests, weeds, and pathogens in agroecosystems. However, the preventative pest management tactics that dominate field-crop production in the United States do not promote biological control. In this review, we argue that by reducing disturbance, mitigating the effects of necessary field activities, and controlling pests within an Integrated Pest Management framework, farmers can facilitate the diversity and activity of native and exotic arthropod predators.

An improved high throughput sequencing method for studying oomycete communities.

Culture-independent studies using next generation sequencing have revolutionized microbial ecology, however, oomycete ecology in soils is severely lagging behind. The aim of this study was to improve and validate standard techniques for using high throughput sequencing as a tool for studying oomycete communities. The well-known primer sets ITS4, ITS6 and ITS7 were used in the study in a semi-nested PCR approach to target the internal transcribed spacer (ITS) 1 of ribosomal DNA in a next generation sequencing protocol. These primers have been used in similar studies before, but with limited success. We were able to increase the proportion of retrieved oomycete sequences dramatically mainly by increasing the annealing temperature during PCR. The optimized protocol was validated using three mock communities and the method was further evaluated using total DNA from 26 soil samples collected from different agricultural fields in Denmark, and 11 samples from carrot tissue with symptoms of Pythium infection. Sequence data from the Pythium and Phytophthora mock communities showed that our strategy successfully detected all included species. Taxonomic assignments of OTUs from 26 soil sample showed that 95% of the sequences could be assigned to oomycetes including Pythium, Aphanomyces, Peronospora, Saprolegnia and Phytophthora. A high proportion of oomycete reads was consistently present in all 26 soil samples showing the versatility of the strategy. A large diversity of Pythium species including pathogenic and saprophytic species were dominating in cultivated soil. Finally, we analyzed amplicons from carrots with symptoms of cavity spot. This resulted in 94% of the reads belonging to oomycetes with a dominance of species of Pythium that are known to be involved in causing cavity spot, thus demonstrating the usefulness of the method not only in soil DNA but also in a plant DNA background. In conclusion, we demonstrate a successful approach for pyrosequencing of oomycete communities using ITS1 as the barcode sequence with well-known primers for oomycete DNA amplification.

A metagenomics-based approach to the top-down effect on the detritivore food web: a salamanders influence on fungal communities within a deciduous forest.

The flow of energy within an ecosystem can be considered either top-down, where predators influence consumers, or bottom-up, where producers influence consumers. Plethodon cinereus (Red-backed Salamander) is a terrestrial keystone predator who feeds on invertebrates within the ecosystem. We investigated the impact of the removal of P. cinereus on the detritivore food web in an upland deciduous forest in northwest Ohio, U.S.A. A total of eight aluminum enclosures, each containing a single P. cinereus under a small log, were constructed in the deciduous forest. On Day 1 of the experiment, four salamanders were evicted from four of the eight enclosures. Organic matter and soil were collected from the center of each enclosure at Day 1 and Day 21. From each sample, DNA was extracted, fungal-specific amplification performed, and 454 pyrosequencing was used to sequence the nuclear ribosomal internal transcribed spacer (ITS2) region and partial ribosomal large subunit (LSU). Changes in overall fungal community composition or species diversity were not statistically significant between treatments. Statistically significant shifts in the most abundant taxonomic groups of fungi were documented in presence but not absence enclosures. We concluded that P. cinereus does not affect the overall composition or diversity of fungal communities, but does have an impact on specific groups of fungi. This study used a metagenomics-based approach to investigate a missing link among a keystone predator, P. cinereus, invertebrates, and fungal communities, all of which are critical in the detritivore food web.