Soil nematode abundance and functional group composition at a global scale.

Soil organisms are a crucial part of the terrestrial biosphere. Despite their importance for ecosystem functioning, few quantitative, spatially explicit models of the active belowground community currently exist. In particular, nematodes are the most abundant animals on Earth, filling all trophic levels in the soil food web. Here we use 6,759 georeferenced samples to generate a mechanistic understanding of the patterns of the global abundance of nematodes in the soil and the composition of their functional groups. The resulting maps show that 4.4 ± 0.64 × 1020 nematodes (with a total biomass of approximately 0.3 gigatonnes) inhabit surface soils across the world, with higher abundances in sub-Arctic regions (38% of total) than in temperate (24%) or tropical (21%) regions. Regional variations in these global trends also provide insights into local patterns of soil fertility and functioning. These high-resolution models provide the first steps towards representing soil ecological processes in global biogeochemical models and will enable the prediction of elemental cycling under current and future climate scenarios.

Spores of arbuscular mycorrhizal fungi host surprisingly diverse communities of endobacteria.

Arbuscular mycorrhizal fungi (AMF) are ubiquitous plant root symbionts, which can house two endobacteria: Ca. Moeniiplasma glomeromycotorum (CaMg) and Ca. Glomeribacter gigasporarum (CaGg). However, little is known about their distribution and population structure in natural AMF populations and whether AMF can harbour other endobacteria. We isolated AMF from two environments and conducted detailed analyses of endobacterial communities associated with surface-sterilised AMF spores. Consistent with the previous reports, we found that CaMg were extremely abundant (80%) and CaGg were extremely rare (2%) in both environments. Unexpectedly, we discovered an additional and previously unknown level of bacterial diversity within AMF spores, which extended beyond the known endosymbionts, with bacteria belonging to 10 other phyla detected across our spore data set. Detailed analysis revealed that: CaGg were not limited in distribution to the Gigasporaceae family of AMF, as previously thought; CaMg population structure was driven by AMF host genotype; and a significant inverse correlation existed between the diversity of CaMg and diversity of all other endobacteria. Based on these data, we generate novel testable hypotheses regarding the function of CaMg in AMF biology by proposing that they might act as conditional mutualists of AMF.

Evidence of a selective and bi-directional relationship between arbuscular mycorrhizal fungal and bacterial communities co-inhabiting plant roots.

Arbuscular mycorrhizal fungi (AMF) provide plants with vital mineral nutrients and co-exist inside the roots alongside a complex community of bacterial endophytes. These co-existing AMF and bacterial root communities have been studied individually and are known to be influenced in structure by different environmental parameters. However, the extent to which they are affected by environmental parameters and by each other is completely unknown. The current study addressed this knowledge gap by characterising AMF and bacterial communities inside plant roots from a natural and an agricultural ecosystem. Using multivariate modelling, the relative contribution of environmental parameters in structuring the two communities was quantified at different spatial scales. Using this model, it was possible to then remove the contribution of environmental parameters and show that the co-existing AMF and bacterial communities were significantly correlated with each other, explaining up to 36% of each other's variance. Notably, this was not due to the presence of know AMF endobacteria, as removal of endobacterial reads maintained the significance of correlation. These findings provide the first empirical evidence of a selective and bi-directional relationship between AMF and bacteria co-inhibiting plant roots and indicate that a significant fraction of this covariation is due to biological and ecological interactions between them.

Population asynchrony alone does not explain stability in species-rich soil animal assemblages: The stabilizing role of forest age on oribatid mite communities.

The importance of microbial and plant communities in the control of the diversity and structure of soil animal communities has been clarified over the last decade. Previous research focused on abiotic factors, niche separation and spatial patterns. Significant gaps still exist in our knowledge of the factors that control the stability of these communities over time. We analysed a 9-year dataset from the national Long-term Ecological Research Network of Latvia. We focused on 117 oribatid species from three Scots pine forests of different age (<40, 65 and >150 years) and structure. For each forest type, 100 samples were collected each year, providing very high replication and long time series for a soil community. We assessed different aspects of stability: we used a dynamic null model, parameterized on observed growth rates, to test the hypothesis that asynchrony in species populations stabilizes total community size; we also analysed alpha and beta diversity over time to test the hypothesis that temporal variation in species composition and relative abundances is controlled by forest attributes. Real communities can be more stable than their stochastic counterparts if species are asynchronous, confirming for the first time the role of asynchrony in stabilizing soil communities. Yet, while some real communities were more stable and had higher abundance and growth rates than others, they were not necessarily more asynchronous than the less stable communities. Species composition and relative abundances were also less variable in the more stable communities. Species asynchrony generally stabilizes species-rich communities but is not sufficient to explain the different levels of stability between forests. Forest age is a key factor explaining the different levels of overyielding and so stability. Data suggest that both asynchrony and high diversity of microhabitat structure of Scots pine forests promote the stability of soil animal communities.

Plastics everywhere: first evidence of polystyrene fragments inside the common Antarctic collembolan Cryptopygus antarcticus.

There is evidence and serious concern that microplastics have reached the most remote regions of the planet, but how far have they travelled in terrestrial ecosystems? This study presents the first field-based evidence of plastic ingestion by a common and central component of Antarctic terrestrial food webs, the collembolan Cryptopygus antarcticus. A large piece of polystyrene (PS) foam (34 × 31 × 5 cm) covered by microalgae, moss, lichens and microfauna was found in a fellfield along the shores of the Fildes Peninsula (King George Island). The application of an improved enzymatic digestion coupled with Fourier transform infrared microscopy (µ-FTIR), unequivocally detected traces of PS (less than 100 µm) in the gut of the collembolans associated with the PS foam and documented their ability to ingest plastic. Plastics are thus entering the short Antarctic terrestrial food webs and represent a new potential stressor to polar ecosystems already facing climate change and increasing human activities. Future research should explore the effects of plastics on the composition, structure and functions of polar terrestrial biota.

Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity.

Theory suggests that more complex food webs promote stability and can buffer the effects of perturbations, such as drought, on soil organisms and ecosystem functions. Here, we tested experimentally how soil food web trophic complexity modulates the response to drought of soil functions related to carbon cycling and the capture and transfer below-ground of recent photosynthate by plants. We constructed experimental systems comprising soil communities with one, two or three trophic levels (microorganisms, detritivores and predators) and subjected them to drought. We investigated how food web trophic complexity in interaction with drought influenced litter decomposition, soil CO2 efflux, mycorrhizal colonization, fungal production, microbial communities and soil fauna biomass. Plants were pulse-labelled after the drought with 13 C-CO2 to quantify the capture of recent photosynthate and its transfer below-ground. Overall, our results show that drought and soil food web trophic complexity do not interact to affect soil functions and microbial community composition, but act independently, with an overall stronger effect of drought. After drought, the net uptake of 13 C by plants was reduced and its retention in plant biomass was greater, leading to a strong decrease in carbon transfer below-ground. Although food web trophic complexity influenced the biomass of Collembola and fungal hyphal length, 13 C enrichment and the net transfer of carbon from plant shoots to microbes and soil CO2 efflux were not affected significantly by varying the number of trophic groups. Our results indicate that drought has a strong effect on above-ground-below-ground linkages by reducing the flow of recent photosynthate. Our results emphasize the sensitivity of the critical pathway of recent photosynthate transfer from plants to soil organisms to a drought perturbation, and show that these effects may not be mitigated by the trophic complexity of soil communities, at least at the level manipulated in this experiment.

Historical biome distribution and recent human disturbance shape the diversity of arbuscular mycorrhizal fungi.

The availability of global microbial diversity data, collected using standardized metabarcoding techniques, makes microorganisms promising models for investigating the role of regional and local factors in driving biodiversity. Here we modelled the global diversity of symbiotic arbuscular mycorrhizal (AM) fungi using currently available data on AM fungal molecular diversity (small subunit (SSU) ribosomal RNA (rRNA) gene sequences) in field samples. To differentiate between regional and local effects, we estimated species pools (sets of potentially suitable taxa) for each site, which are expected to reflect regional processes. We then calculated community completeness, an index showing the fraction of the species pool present, which is expected to reflect local processes. We found significant spatial variation, globally in species pool size, as well as in local and dark diversity (absent members of the species pool). Species pool size was larger close to areas containing tropical grasslands during the last glacial maximum, which are possible centres of diversification. Community completeness was greater in regions of high wilderness (remoteness from human disturbance). Local diversity was correlated with wilderness and current connectivity to mountain grasslands. Applying the species pool concept to symbiotic fungi facilitated a better understanding of how biodiversity can be jointly shaped by large-scale historical processes and recent human disturbance.

Priorities for research in soil ecology.

The ecological interactions that occur in and with soil are of consequence in many ecosystems on the planet. These interactions provide numerous essential ecosystem services, and the sustainable management of soils has attracted increasing scientific and public attention. Although soil ecology emerged as an independent field of research many decades ago, and we have gained important insights into the functioning of soils, there still are fundamental aspects that need to be better understood to ensure that the ecosystem services that soils provide are not lost and that soils can be used in a sustainable way. In this perspectives paper, we highlight some of the major knowledge gaps that should be prioritized in soil ecological research. These research priorities were compiled based on an online survey of 32 editors of Pedobiologia - Journal of Soil Ecology. These editors work at universities and research centers in Europe, North America, Asia, and Australia.The questions were categorized into four themes: (1) soil biodiversity and biogeography, (2) interactions and the functioning of ecosystems, (3) global change and soil management, and (4) new directions. The respondents identified priorities that may be achievable in the near future, as well as several that are currently achievable but remain open. While some of the identified barriers to progress were technological in nature, many respondents cited a need for substantial leadership and goodwill among members of the soil ecology research community, including the need for multi-institutional partnerships, and had substantial concerns regarding the loss of taxonomic expertise.

Eating from the same plate? Revisiting the role of labile carbon inputs in the soil food web.

An increasing number of empirical studies are challenging the central fundamentals on which the classical soil food web model is built. This model assumes that bacteria consume labile substrates twice as fast as fungi, and that mycorrhizal fungi do not decompose organic matter. Here, we build on emerging evidence that points to significant consumption of labile C by fungi, and to the ability of ectomycorrhizal fungi to decompose organic matter, to show that labile C constitutes a major and presently underrated source of C for the soil food web. We use a simple model describing the dynamics of a recalcitrant and a labile C pool and their consumption by fungi and bacteria to show that fungal and bacterial populations can coexist in a stable state with large inputs into the labile C pool and a high fungal use of labile C. We propose a new conceptual model for the bottom trophic level of the soil food web, with organic C consisting of a continuous pool rather than two or three distinct pools, and saprotrophic fungi using substantial amounts of labile C. Incorporation of these concepts will increase our understanding of soil food web dynamics and functioning under changing conditions.

Interactive effects of root endophytes and arbuscular mycorrhizal fungi on an experimental plant community.

Plant-soil microbial interactions have moved into focus as an important mechanism for understanding plant coexistence and composition of communities. Both arbuscular mycorrhizal (AM) as well as other root endophytic fungi co-occur in plant roots, and therefore have the potential to influence relative abundances of plant species in local assemblages. However, no study has experimentally examined how these key root endosymbiont groups might interact and affect plant community composition. Here, using an assemblage of five plant species in mesocosms in a fully factorial experiment, we added an assemblage of AM fungi and/or a mixture of root endophytic fungal isolates, all obtained from the same grassland field site. The results demonstrate that the AM fungi and root endophytes interact to affect plant community composition by changing relative species abundance, and consequently aboveground productivity. Our study highlights the need to explicitly consider interactions of root-inhabiting fungal groups in studies of plant assemblages.

Biotic interactions as a structuring force in soil communities: evidence from the micro-arthropods of an Antarctic moss model system.

Current meta-community theories postulate that the structure of local communities depends on dispersal, environmental filtering, and biotic interactions. However, disentangling the relative effects of these factors in the field and for diverse assemblages is a major challenge. A solution is to address natural but simple communities (i.e. with low numbers of species in few trophic levels), wherein one of these factors is predominant. Here, we analyse the micro-arthropod community of a moss-turf habitat typical of the Antarctic Peninsula region, and test the widely accepted hypothesis that this system is abiotically driven. In the austral summers 2006/7 and 2007/8, we sampled nearly 80 units of moss from four islands in the Argentine Islands. Using variance partitioning, we quantified the relative contribution of: (1) multiple scale spatio-temporal autocorrelation; (2) environmental effects; (3) the island effect. Little variance (1 %) was accounted for by sources 1 (1 %, significant) and 2 (<1 %, not significant). The island effect significantly accounted for the largest amount of variation (8 %). There was a relatively large effect of spatially structured environmental variation (7 %). Null models demonstrated that species co-occurred less frequently than expected by chance, suggesting the prevalence of negative interactions. Our data support the novel hypothesis that negative biotic interactions are the most important structuring force of this micro-arthropod community. The analysed system is a good proxy for more complex communities in terms of taxonomic composition and the functional groups present. Thus, biotic interaction might be a predominant factor in soil meta-community dynamics.

Contribution of soil bacteria to the atmosphere across biomes.

The dispersion of microorganisms through the atmosphere is a continual and essential process that underpins biogeography and ecosystem development and function. Despite the ubiquity of atmospheric microorganisms globally, specific knowledge of the determinants of atmospheric microbial diversity at any given location remains unresolved. Here we describe bacterial diversity in the atmospheric boundary layer and underlying soil at twelve globally distributed locations encompassing all major biomes, and characterise the contribution of local and distant soils to the observed atmospheric community. Across biomes the diversity of bacteria in the atmosphere was negatively correlated with mean annual precipitation but positively correlated to mean annual temperature. We identified distinct non-randomly assembled atmosphere and soil communities from each location, and some broad trends persisted across biomes including the enrichment of desiccation and UV tolerant taxa in the atmospheric community. Source tracking revealed that local soils were more influential than distant soil sources in determining observed diversity in the atmosphere, with more emissive semi-arid and arid biomes contributing most to signatures from distant soil. Our findings highlight complexities in the atmospheric microbiota that are relevant to understanding regional and global ecosystem connectivity.

Relative role of deterministic and stochastic determinants of soil animal community: a spatially explicit analysis of oribatid mites.

1. Ecologists are debating the relative role of deterministic and stochastic determinants of community structure. Although the high diversity and strong spatial structure of soil animal assemblages could provide ecologists with an ideal ecological scenario, surprisingly little information is available on these assemblages. 2. We studied species-rich soil oribatid mite assemblages from a Mediterranean beech forest and a grassland. We applied multivariate regression approaches and analysed spatial autocorrelation at multiple spatial scales using Moran's eigenvectors. Results were used to partition community variance in terms of the amount of variation uniquely accounted for by environmental correlates (e.g. organic matter) and geographical position. Estimated neutral diversity and immigration parameters were also applied to a soil animal group for the first time to simulate patterns of community dissimilarity expected under neutrality, thereby testing neutral predictions. 3. After accounting for spatial autocorrelation, the correlation between community structure and key environmental parameters disappeared: about 40% of community variation consisted of spatial patterns independent of measured environmental variables such as organic matter. Environmentally independent spatial patterns encompassed the entire range of scales accounted for by the sampling design (from tens of cm to 100 m). This spatial variation could be due to either unmeasured but spatially structured variables or stochastic drift mediated by dispersal. Observed levels of community dissimilarity were significantly different from those predicted by neutral models. 4. Oribatid mite assemblages are dominated by processes involving both deterministic and stochastic components and operating at multiple scales. Spatial patterns independent of the measured environmental variables are a prominent feature of the targeted assemblages, but patterns of community dissimilarity do not match neutral predictions. This suggests that either niche-mediated competition or environmental filtering or both are contributing to the core structure of the community. This study indicates new lines of investigation for understanding the mechanisms that determine the signature of the deterministic component of animal community assembly.

Primary assembly of soil communities: disentangling the effect of dispersal and local environment.

It has long been recognised that dispersal abilities and environmental factors are important in shaping invertebrate communities, but their relative importance for primary soil community assembly has not yet been disentangled. By studying soil communities along chronosequences on four recently emerged nunataks (ice-free land in glacial areas) in Iceland, we replicated environmental conditions spatially at various geographical distances. This allowed us to determine the underlying factors of primary community assembly with the help of metacommunity theories that predict different levels of dispersal constraints and effects of the local environment. Comparing community assembly of the nunataks with that of non-isolated deglaciated areas indicated that isolation of a few kilometres did not affect the colonisation of the soil invertebrates. When accounting for effects of geographical distances, soil age and plant richness explained a significant part of the variance observed in the distribution of the oribatid mites and collembola communities, respectively. Furthermore, null model analyses revealed less co-occurrence than expected by chance and also convergence in the body size ratio of co-occurring oribatids, which is consistent with species sorting. Geographical distances influenced species composition, indicating that the community is also assembled by dispersal, e.g. mass effect. When all the results are linked together, they demonstrate that local environmental factors are important in structuring the soil community assembly, but are accompanied with effects of dispersal that may "override" the visible effect of the local environment.

"Jack-of-all-trades" is parthenogenetic.

Sex is evolutionarily more costly than parthenogenesis, evolutionary ecologists therefore wonder why sex is much more frequent than parthenogenesis in the majority of animal lineages. Intriguingly, parthenogenetic individuals and species are as common as or even more common than sexuals in some major and putative ancient animal lineages such as oribatid mites and rotifers. Here, we analyzed oribatid mites (Acari: Oribatida) as a model group because these mites are ancient (early Paleozoic), widely distributed around the globe, and include a high number of parthenogenetic species, which often co-exist with sexual oribatid mite species. There is evidence that the reproductive mode is phylogenetically conserved in oribatid mites, which makes them an ideal model to test hypotheses on the relationship between reproductive mode and species' ecological strategies. We used oribatid mites to test the frozen niche variation hypothesis; we hypothesized that parthenogenetic oribatid mites occupy narrow specialized ecological niches. We used the geographic range of species as a proxy for specialization as specialized species typically do have narrower geographic ranges than generalistic species. After correcting for phylogenetic signal in reproductive mode and demonstrating that geographic range size has no phylogenetic signal, we found that parthenogenetic lineages have a higher probability to have broader geographic ranges than sexual species arguing against the frozen niche variation hypothesis. Rather, the results suggest that parthenogenetic oribatid mite species are more generalistic than sexual species supporting the general-purpose genotype hypothesis. The reason why parthenogenetic oribatid mite species are generalists with wide geographic range sizes might be that they are of ancient origin reflecting that they adapted to varying environmental conditions during evolutionary history. Overall, our findings indicate that parthenogenetic oribatid mite species possess a widely adapted general-purpose genotype and therefore might be viewed as "Jack-of-all-trades."

Intensive grassland management disrupts below-ground multi-trophic resource transfer in response to drought.

Modification of soil food webs by land management may alter the response of ecosystem processes to climate extremes, but empirical support is limited and the mechanisms involved remain unclear. Here we quantify how grassland management modifies the transfer of recent photosynthates and soil nitrogen through plants and soil food webs during a post-drought period in a controlled field experiment, using in situ 13C and 15N pulse-labelling in intensively and extensively managed fields. We show that intensive management decrease plant carbon (C) capture and its transfer through components of food webs and soil respiration compared to extensive management. We observe a legacy effect of drought on C transfer pathways mainly in intensively managed grasslands, by increasing plant C assimilation and 13C released as soil CO2 efflux but decreasing its transfer to roots, bacteria and Collembola. Our work provides insight into the interactive effects of grassland management and drought on C transfer pathways, and highlights that capture and rapid transfer of photosynthates through multi-trophic networks are key for maintaining grassland resistance to drought.

Local stability properties of complex, species-rich soil food webs with functional block structure.

Ecologists have long debated the properties that confer stability to complex, species-rich ecological networks. Species-level soil food webs are large and structured networks of central importance to ecosystem functioning. Here, we conducted an analysis of the stability properties of an up-to-date set of theoretical soil food web models that account both for realistic levels of species richness and the most recent views on the topological structure (who is connected to whom) of these food webs. The stability of the network was best explained by two factors: strong correlations between interaction strengths and the blocked, nonrandom trophic structure of the web. These two factors could stabilize our model food webs even at the high levels of species richness that are typically found in soil, and that would make random systems very unstable. Also, the stability of our soil food webs is well-approximated by the cascade model. This result suggests that stability could emerge from the hierarchical structure of the functional organization of the web. Our study shows that under the assumption of equilibrium and small perturbations, theoretical soil food webs possess a topological structure that allows them to be complex yet more locally stable than their random counterpart. In particular, results strongly support the general hypothesis that the stability of rich and complex soil food webs is mostly driven by correlations in interaction strength and the organization of the soil food web into functional groups. The implication is that in real-world food web, any force disrupting the functional structure and distribution pattern of interaction strengths (i.e., energy fluxes) of the soil food webs will destabilize the dynamics of the system, leading to species extinction and major changes in the relative abundances of species.

Soil microbial community responses to climate extremes: resistance, resilience and transitions to alternative states.

A major challenge for advancing our understanding of the functional role of soil microbial communities is to link changes in their structure and function under climate change. To address this challenge requires new understanding of the mechanisms that underlie the capacity of soil microbial communities to resist and recover from climate extremes. Here, we synthesize emerging understanding of the intrinsic and extrinsic factors that influence the resistance and resilience of soil microbial communities to climate extremes, with a focus on drought, and identify drivers that might trigger abrupt changes to alternative states. We highlight research challenges and propose a path for advancing our understanding of the resistance and resilience of soil microbial communities to climate extremes, and of their vulnerability to transitions to alternative states, including the use of trait-based approaches. We identify a need for new approaches to quantify resistance and resilience of soil microbial communities, and to identify thresholds for transitions to alternative states. We show how high-resolution time series coupled with gradient designs will enable detecting response patterns to interacting drivers. Finally, to account for extrinsic factors, we suggest that future studies should use environmental gradients to track soil microbial community responses to climate extremes in space and time. This article is part of the theme issue 'Climate change and ecosystems: threats, opportunities and solutions'.

Improving phosphorus sustainability in intensively managed grasslands: The potential role of arbuscular mycorrhizal fungi.

Long-term nutrient fertilization of grassland soils greatly increases plant yields but also profoundly alters ecosystem phosphorus (P) dynamics. Here, we addressed how long-term P fertilization may affect ecosystem P budget, P use efficiency (PUE) and the abundance of arbuscular mycorrhizal fungi (AMF), which play a key role in the acquisition of P by plants. We found that 47 years of organic P applications increased soil P availability and total soil P stocks up to 1600% and 400%, respectively, compared to unfertilized-control soils. Grassland soils could retain up to 62% and 48% of P applied since 1970 in organic and inorganic forms, respectively. Nutrient treatments significantly affected rates of AMF root colonization (%), which were higher in control and NPK-fertilized plots when compared to soils receiving increasing applications of organic P. Plant PUE increased with greater AMF root colonization, which remained high (i.e. 50-to-75%) even after ~50 years of continuous 'normal' rates of agronomic P inputs (~30 kg P ha-1 year-1). AMF abundance, however, decreased under higher P applications and we found a negative relationship between soil P availability or soil P stocks and rates of AMF root colonization. Our study demonstrates that (1) AMF root colonization is still high in soils, which have received consistent but moderate P inputs for over four decades, and (2) moderate rates of P fertilization are related to a more conservative P ecosystem budget whereby the amount of P retained in soils and up-taken by plants on an annual basis is higher than the amount of P added through fertilization. This is possible only if extra P is 'mined' from the soil P 'bank' and made available to plant uptake. We suggest that AMF could play a significant role in intensively-managed grasslands contributing to increase P sustainability by reducing the need for extra P fertilizer.