Root diameter, host specificity and arbuscular mycorrhizal fungal community composition among native and exotic plant species.

Plant root systems rely on a functionally diverse range of arbuscular mycorrhizal fungi to, among other benefits, extend their nutrient foraging. Extended nutrient foraging is likely of greatest importance to coarse-rooted plants, yet few studies have examined the link between root traits and arbuscular mycorrhizal fungal community composition. Here, we examine the relationship between root diameter and the composition of arbuscular mycorrhizal fungal communities in a range of native and exotic plant species. We characterized the arbuscular mycorrhizal fungal communities of 30 co-occurring native and exotic montane grassland/shrubland plant species in New Zealand. We found that plant root diameter and native/exotic status both strongly correlated with arbuscular mycorrhizal fungal community composition. Coarse-rooted plants had a lower diversity of mycorrhizal fungi compared with fine-rooted plants and associated less with generalist fungal partners. Exotic plants had a lower diversity of fungi and fewer associations with nondominant families of arbuscular mycorrhizal fungi compared with native plants. These observational patterns suggest that plants may differentially associate with fungal partners based on their root traits, with coarse-rooted plants being more specific in their associations. Furthermore, exotic plants may associate with dominant arbuscular mycorrhizal fungal taxa as a strategy in invasion.

Environmental and plant community drivers of plant pathogen composition and richness.

Interactions between individual plant pathogens and their environment have been described many times. However, the relative contribution of different environmental parameters as controls of pathogen communities remains largely unknown. Here we investigate the importance of environmental factors, including geomorphology, climate, land use, soil and plant community composition, for a broad range of aboveground and belowground fungal, oomycete and bacterial plant pathogens. We found that plant community composition is the main driver of the composition and richness of plant pathogens after taking into account all other tested parameters, especially those related to climate and soil. In the face of future changes in climate and land use, our results suggest that changes in plant pathogen community composition and richness will primarily be mediated through changes in plant communities, rather than the direct effects of climate or soils.

Agricultural land-use favours Mucoromycotinian, but not Glomeromycotinian, arbuscular mycorrhizal fungi across ten biomes.

Globally, agricultural land-use negatively affects soil biota that contribute to ecosystem functions such as nutrient cycling, yet arbuscular mycorrhizal fungi (AMF) are promoted as essential components of agroecosystems. Arbuscular mycorrhizal fungi include Glomeromycotinian AMF (G-AMF) and the arbuscule-producing fine root endophytes, recently re-classified into the Endogonales order within Mucoromycotina. The correct classification of Mucoromycotinian AMF (M-AMF) and the availability of new molecular tools can guide research to better the understanding of their diversity and ecology. To investigate the impact on G-AMF and M-AMF of agricultural land-use at a continental scale, we sampled DNA from paired farm and native sites across 10 Australian biomes. Glomeromycotinian AMF were present in both native and farm sites in all biomes. Putative M-AMF were favoured by farm sites, rare or absent in native sites, and almost entirely absent in tropical biomes. Temperature, rainfall, and soil pH were strong drivers of richness and community composition of both groups, and plant richness was an important mediator. Both fungal groups occupy different, but overlapping, ecological niches, with M-AMF thriving in temperate agricultural landscapes. Our findings invite exploration of the origin and spread of M-AMF and continued efforts to resolve the phylogeny of this newly reclassified group of AMF.

Soil sample pooling generates no consistent inference bias: a meta-analysis of 71 plant-soil feedback experiments.

There is current debate on how soil sample pooling affects the measurement of plant-soil feedbacks. Several studies have suggested that pooling soil samples among experimental units reduces variance and can bias estimates of plant-soil feedbacks. However, it is unclear whether pooling has resulted in systematic mismeasurement of plant-soil feedbacks in the literature. Using data from 71 experiments, we tested whether pairwise plant-soil feedback direction, magnitude and variance differed among soil pooling treatments. We also tested whether pooling has altered our understanding of abiotic and biotic drivers that influence pairwise plant-soil feedbacks. Pooling of soil samples among experimental units was used in 42% of examined experiments. Contrary to predictions, pooling did not affect mean pairwise plant-soil feedback effect size or within-experiment variance. Accounting for soil sample pooling also did not significantly alter our understanding of the drivers of pairwise plant-soil feedbacks. We conclude that there is no evidence that soil sample pooling systematically biases estimates of plant-soil feedback direction, magnitude, variance or drivers across many studies. Given the debate of whether to pool soil samples, researchers should be aware of potential criticisms and carefully consider how experimental design and soil pooling methods influence interpretation of experiments.

Evidence for Niche Differentiation in the Environmental Responses of Co-occurring Mucoromycotinian Fine Root Endophytes and Glomeromycotinian Arbuscular Mycorrhizal Fungi.

Fine root endophytes (FRE) were traditionally considered a morphotype of arbuscular mycorrhizal fungi (AMF), but recent genetic studies demonstrate that FRE belong within the subphylum Mucoromycotina, rather than in the subphylum Glomeromycotina with the AMF. These findings prompt enquiry into the fundamental ecology of FRE and AMF. We sampled FRE and AMF in roots of Trifolium subterraneum from 58 sites across temperate southern Australia. We investigated the environmental drivers of composition, richness, and root colonization of FRE and AMF by using structural equation modelling and canonical correspondence analyses. Root colonization by FRE increased with increasing temperature and rainfall but decreased with increasing phosphorus (P). Root colonization by AMF increased with increasing soil organic carbon but decreased with increasing P. Richness of FRE decreased with increasing temperature and soil pH. Richness of AMF increased with increasing temperature and rainfall but decreased with increasing soil aluminium (Al) and pH. Aluminium, soil pH, and rainfall were, in decreasing order, the strongest drivers of community composition of FRE; they were also important drivers of community composition of AMF, along with temperature, in decreasing order: rainfall, Al, temperature, and soil pH. Thus, FRE and AMF showed the same responses to some (e.g. soil P, soil pH) and different responses to other (e.g. temperature) key environmental factors. Overall, our data are evidence for niche differentiation among these co-occurring mycorrhizal associates.

Dual-mycorrhizal plants: their ecology and relevance.

Dual-mycorrhizal plants are capable of associating with fungi that form characteristic arbuscular mycorrhizal (AM) and ectomycorrhizal (EM) structures. Here, we address the following questions: (1) How many dual-mycorrhizal plant species are there? (2) What are the advantages for a plant to host two, rather than one, mycorrhizal types? (3) Which factors can provoke shifts in mycorrhizal dominance (i.e. mycorrhizal switching)? We identify a large number (89 genera within 32 families) of confirmed dual-mycorrhizal plants based on observing arbuscules or coils for AM status and Hartig net or similar structures for EM status within the same plant species. We then review the possible nutritional benefits and discuss the possible mechanisms leading to net costs and benefits. Cost and benefits of dual-mycorrhizal status appear to be context dependent, particularly with respect to the life stage of the host plant. Mycorrhizal switching occurs under a wide range of abiotic and biotic factors, including soil moisture and nutrient status. The relevance of dual-mycorrhizal plants in the ecological restoration of adverse sites where plants are not carbon limited is discussed. We conclude that dual-mycorrhizal plants are underutilized in ecophysiological-based experiments, yet are powerful model plant-fungal systems to better understand mycorrhizal symbioses without confounding host effects.

Rare species of wood-inhabiting fungi are not local.

Wood-inhabiting fungal communities are a diverse and ecologically critical part of forest ecosystems, yet the spatial structure of fungal biodiversity in these ecosystems is largely unknown. Legislation allowed harvesting of deadwood from temperate rainforests on conservation lands in New Zealand following Cyclone Ita in 2014. Harvesting guidelines specified widely spread harvesting, on the assumption that rare fungal species may be highly spatially restricted, but were not based on quantitative assessment. We sampled fungi in and on logs of Dacrydium cupressinum (Podocarpaceae) a long-lived, common, canopy tree in lowland New Zealand forests. DNA was extracted from 81 logs varying in decay state across a 40 km long region of West Coast (South Island) forests, and sequenced using general fungal primers for metabarcoding to identify OTUs (operational taxonomic units). We examined three axes of rarity: occupancy, dominance when present, and niche breadth (as spatial extent and decay state specialization). Low-occupancy fungi were common, including a group of infrequently occurring but dominant when present fungi, the majority of which were Ascomycota. Despite this, there was an overall positive relationship between occupancy and dominance. Widespread, dominant fungi were most commonly Basidiomycota. Testing all fungal OTUs, there were no more fungi with maximum range sizes < 4 km than would be expected at random. Of the 351 low-occupancy OTUs found two to four times, only 12 had maximum range sizes < 900 m, and there was no more spatial restriction at scales < 900 m than would be expected by random chance, although there was some evidence of niche breadth restriction based on decay state similarity. The results show that fungal communities in deadwood are highly diverse, and include many rare taxa. Nonetheless, the lack of fungal OTUs with spatial restriction at scales < 900 m suggests that spatially dispersed timber harvesting will not mitigate risks of harvesting to rare fungal biodiversity.

Potential and limitation of air pollution mitigation by vegetation and uncertainties of deposition-based evaluations.

The potential to capture additional air pollutants by introducing more vegetation or changing existing short vegetation to woodland on first sight provides an attractive route for lowering urban pollution. Here, an atmospheric chemistry and transport model was run with a range of landcover scenarios to quantify pollutant removal by the existing total UK vegetation as well as the UK urban vegetation and to quantify the effect of large-scale urban tree planting on urban air pollution. UK vegetation as a whole reduces area (population)-weighted concentrations significantly, by 10% (9%) for PM2.5, 30% (22%) for SO2, 24% (19%) for NH3 and 15% (13%) for O3, compared with a desert scenario. By contrast, urban vegetation reduces average urban PM2.5 by only approximately 1%. Even large-scale conversion of half of existing open urban greenspace to forest would lower urban PM2.5 by only another 1%, suggesting that the effect on air quality needs to be considered in the context of the wider benefits of urban tree planting, e.g. on physical and mental health. The net benefits of UK vegetation for NO2 are small, and urban tree planting is even forecast to increase urban NO2 and NOx concentrations, due to the chemical interaction with changes in BVOC emissions and O3, but the details depend on tree species selection. By extrapolation, green infrastructure projects focusing on non-greenspace (roadside trees, green walls, roof-top gardens) would have to be implemented at very large scales to match this effect. Downscaling of the results to micro-interventions solely aimed at pollutant removal suggests that their impact is too limited for their cost-benefit analysis to compare favourably with emission abatement measures. Urban vegetation planting is less effective for lowering pollution than measures to reduce emissions at source. The results highlight interactions that cannot be captured if benefits are quantified via deposition models using prescribed concentrations, and emission damage costs. This article is part of a discussion meeting issue 'Air quality, past present and future'.

Land use is a determinant of plant pathogen alpha- but not beta-diversity.

Little is known about the diversity patterns of plant pathogens and how they change with land use at a broad scale. We employed DNA metabarcoding to describe the diversity and composition of putative plant pathogen communities in three substrates (soil, roots, and leaves) across five major land uses at a national scale. Almost all plant pathogen communities (fungi, oomycetes, and bacteria) showed strong responses to land use and substrate type. Land use category could explain up to 24% of the variance in composition between communities. Alpha-diversity (richness) of plant pathogens was consistently lower in natural forests than in agricultural systems. In planted forests, there was also generally low pathogen alpha-diversity in soil and roots, but alpha-diversity in leaves was high compared with most other land uses. In contrast to alpha-diversity, differences in within-land use beta-diversity of plant pathogens (the predictability of plant pathogen communities within land use) were subtle. Our results show that large-scale patterns and distributions of putative plant pathogens can be determined using metabarcoding, allowing some of the first landscape level insights into these critically important communities.

Contrasting responses of soil nematode communities to native and non-native woody plant expansion.

Woody plant expansion into grasslands is widespread, driven by both successions to dominance by native woody species or invasion by non-native woody species. These shifts from grass- to woody-dominated systems also have profound effects on both above- and belowground communities and ecosystem processes. Woody-plant expansion should also alter the functional composition of the soil biota, including that of nematodes, which are major drivers of soil food-web structure and belowground processes, but such belowground impacts are poorly understood. We determined whether succession by a widespread native (Kunzea ericoides) and invasion by a non-native woody species (Pinus nigra) into tussock grasslands affect the composition of nematode functional guilds and the structure of nematode-based food webs. Although increasing dominance by woody species in both systems altered the functional guild composition of the nematode community, we found contrasting responses of nematode functional guilds to the different dominant plant species. Specifically, nematode communities reflected conditions of resource enrichment with increasing K. ericoides tree cover, whereas communities became structurally simplified and dominated by stress-tolerant nematode families with increasing P. nigra tree cover. Because nematodes regulate both bacterial- and fungal-dominated food webs in soils, these shifts could in turn alter multiple ecosystem processes belowground such as nutrient cycling. Incorporating species' functional traits into the assessment of habitat-change impacts on communities can greatly improve our understanding of species responses to environmental changes and their consequences in ecosystems.

Symmetric assembly and disassembly processes in an ecological network.

The processes whereby ecological networks emerge, persist and decay throughout ecosystem development are largely unknown. Here we study networks of plant and arbuscular mycorrhizal fungal (AMF) communities along a 120 000 year soil chronosequence, as they undergo assembly (progression) and then disassembly (retrogression). We found that network assembly and disassembly were symmetrical, self-reinforcing processes that together were capable of generating key attributes of network architecture. Plant and AMF species that had short indirect paths to others in the community (i.e. high centrality), rather than many direct interaction partners (i.e. high degree), were best able to attract new interaction partners and, in the case of AMF species, also to retain existing interactions with plants during retrogression. We then show using simulations that these non-random patterns of attachment and detachment promote nestedness of the network. These results have implications for predicting extinction sequences, identifying focal points for invasions and suggesting trajectories for restoration.

Priority effects are interactively regulated by top-down and bottom-up forces: evidence from wood decomposer communities.

Both top-down (grazing) and bottom-up (resource availability) forces can determine the strength of priority effects, or the effects of species arrival history on the structure and function of ecological communities, but their combined influences remain unresolved. To test for such influences, we assembled experimental communities of wood-decomposing fungi using a factorial manipulation of fungivore (Folsomia candida) presence, nitrogen availability, and fungal assembly history. We found interactive effects of all three factors on fungal species composition and wood decomposition 1 year after the fungi were introduced. The strength of priority effects on community structure was affected primarily by nitrogen availability, whereas the strength of priority effects on decomposition rate was interactively regulated by nitrogen and fungivores. These results demonstrate that top-down and bottom-up forces jointly determine how strongly assembly history affects community structure and function.

The emerging science of linked plant-fungal invasions.

Contents 1314 I. 1315 II. 1316 III. 1322 IV. 1323 V. 1325 VI. 1326 VII. 1326 VIII. 1327 1328 References 1328 SUMMARY: Invasions of alien plants are typically studied as invasions of individual species, yet interactions between plants and symbiotic fungi (mutualists and potential pathogens) affect plant survival, physiological traits, and reproduction and hence invasion success. Studies show that plant-fungal associations are frequently key drivers of plant invasion success and impact, but clear conceptual frameworks and integration across studies are needed to move beyond a series of case studies towards a more predictive understanding. Here, we consider linked plant-fungal invasions from the perspective of plant and fungal origin, simplified to the least complex representations or 'motifs'. By characterizing these interaction motifs, parallels in invasion processes between pathogen and mutualist fungi become clear, although the outcomes are often opposite in effect. These interaction motifs provide hypotheses for fungal-driven dynamics behind observed plant invasion trajectories. In some situations, the effects of plant-fungal interactions are inconsistent or negligible. Variability in when and where different interaction motifs matter may be driven by specificity in the plant-fungal interaction, the size of the effect of the symbiosis (negative to positive) on plants and the dependence (obligate to facultative) of the plant-fungal interaction. Linked plant-fungal invasions can transform communities and ecosystem function, with potential for persistent legacies preventing ecosystem restoration.

Fine root endophytes under scrutiny: a review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina.

Fine root endophytes (FRE) are arbuscule-forming fungi presently considered as a single species-Glomus tenue in the Glomeromycota (Glomeromycotina)-but probably belong within the Mucoromycotina. Thus, FRE are the only known arbuscule-forming fungi not within the arbuscular mycorrhizal fungi (AMF; Glomeromycotina) as currently understood. Phylogenetic differences between FRE and AMF could reflect ecological differences. To synthesize current ecological knowledge, we reviewed the literature on FRE and identified 108 papers that noted the presence of FRE and, in some, the colonization levels for FRE or AMF (or both). We categorized these records by geographic region, host-plant family and environment (agriculture, moderate-natural, low-temperature, high-altitude and other) and determined their influence on the percentage of root length colonized by FRE in a meta-analysis. We found that FRE are globally distributed, with many observations from Poaceae, perhaps due to grasses being widely distributed. In agricultural environments, colonization by FRE often equalled or exceeded that of AMF, particularly in Australasia. In moderate-natural and high-altitude environments, average colonization by FRE (~10%) was lower than that of AMF (~35%), whereas in low-temperature environments, colonization was similar (~20%). Several studies suggested that FRE can enhance host-plant phosphorus uptake and growth, and may be more resilient than AMF to environmental stress in some host plants. Further research is required on the functioning of FRE in relation to the environment, host plant and co-occurring AMF and, in particular, to examine whether FRE are important for plant growth in stressful environments. Targeted molecular primers are urgently needed for further research on FRE.

Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development.

Little is known about the response of arbuscular mycorrhizal fungal communities to ecosystem development. We use a long-term soil chronosequence that includes ecosystem progression and retrogression to quantify the importance of host plant identity as a factor driving fungal community composition during ecosystem development. We identified arbuscular mycorrhizal fungi and plant species from 50 individual roots from each of 10 sites spanning 5-120 000 yr of ecosystem age using terminal restriction fragment length polymorphism (T-RFLP), Sanger sequencing and pyrosequencing. Arbuscular mycorrhizal fungal communities were highly structured by ecosystem age. There was strong niche differentiation, with different groups of operational taxonomic units (OTUs) being characteristic of early succession, ecosystem progression and ecosystem retrogression. Fungal alpha diversity decreased with ecosystem age, whereas beta diversity was high at early stages and lower in subsequent stages. A total of 39% of the variance in fungal communities was explained by host plant and site age, 29% of which was attributed to host and the interaction between host and site (24% and 5%, respectively). The strong response of arbuscular mycorrhizal fungi to ecosystem development appears to be largely driven by plant host identity, supporting the concept that plant and fungal communities are tightly coupled rather than independently responding to habitat.

Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes.

Fine roots acquire essential soil resources and mediate biogeochemical cycling in terrestrial ecosystems. Estimates of carbon and nutrient allocation to build and maintain these structures remain uncertain because of the challenges of consistently measuring and interpreting fine-root systems. Traditionally, fine roots have been defined as all roots ≤ 2 mm in diameter, yet it is now recognized that this approach fails to capture the diversity of form and function observed among fine-root orders. Here, we demonstrate how order-based and functional classification frameworks improve our understanding of dynamic root processes in ecosystems dominated by perennial plants. In these frameworks, fine roots are either separated into individual root orders or functionally defined into a shorter-lived absorptive pool and a longer-lived transport fine-root pool. Using these frameworks, we estimate that fine-root production and turnover represent 22% of terrestrial net primary production globally - a c. 30% reduction from previous estimates assuming a single fine-root pool. Future work developing tools to rapidly differentiate functional fine-root classes, explicit incorporation of mycorrhizal fungi into fine-root studies, and wider adoption of a two-pool approach to model fine roots provide opportunities to better understand below-ground processes in the terrestrial biosphere.

Mycorrhizal co-invasion and novel interactions depend on neighborhood context.

Biological invasions are a rapidly increasing driver of global change, yet fundamental gaps remain in our understanding of the factors determining the success or extent of invasions. For example, although most woody plant species depend on belowground mutualists such as mycorrhizal fungi and nitrogen-fixing bacteria, the relative importance of these mutualisms in conferring invasion success is unresolved. Here, we describe how neighborhood context (identity of nearby tree species) affects the formation of belowground ectomycorrhizal partnerships between fungi and seedlings of a widespread invasive tree species, Pseudotsuga menziesii (Douglas-fir), in New Zealand. We found that the formation of mycorrhizal partnerships, the composition of the fungal species involved in these partnerships, and the origin of the fungi (co-invading or native to New Zealand) all depend on neighborhood context. Our data suggest that nearby ectomycorrhizal host trees act as both a reservoir of fungal inoculum and a carbon source for late-successional and native fungi. By facilitating mycorrhization of P. menziesii seedlings, adult trees may alleviate mycorrhizal limitation at the P. menziesii invasion front. These results highlight the importance of studying biological invasions across multiple ecological settings to understand establishment success and invasion speed.

Effects of climate change on the delivery of soil-mediated ecosystem services within the primary sector in temperate ecosystems: a review and New Zealand case study.

Future human well-being under climate change depends on the ongoing delivery of food, fibre and wood from the land-based primary sector. The ability to deliver these provisioning services depends on soil-based ecosystem services (e.g. carbon, nutrient and water cycling and storage), yet we lack an in-depth understanding of the likely response of soil-based ecosystem services to climate change. We review the current knowledge on this topic for temperate ecosystems, focusing on mechanisms that are likely to underpin differences in climate change responses between four primary sector systems: cropping, intensive grazing, extensive grazing and plantation forestry. We then illustrate how our findings can be applied to assess service delivery under climate change in a specific region, using New Zealand as an example system. Differences in the climate change responses of carbon and nutrient-related services between systems will largely be driven by whether they are reliant on externally added or internally cycled nutrients, the extent to which plant communities could influence responses, and variation in vulnerability to erosion. The ability of soils to regulate water under climate change will mostly be driven by changes in rainfall, but can be influenced by different primary sector systems' vulnerability to soil water repellency and differences in evapotranspiration rates. These changes in regulating services resulted in different potentials for increased biomass production across systems, with intensively managed systems being the most likely to benefit from climate change. Quantitative prediction of net effects of climate change on soil ecosystem services remains a challenge, in part due to knowledge gaps, but also due to the complex interactions between different aspects of climate change. Despite this challenge, it is critical to gain the information required to make such predictions as robust as possible given the fundamental role of soils in supporting human well-being.