Mycorrhizal type of woody plants influences understory species richness in British broadleaved woodlands.

Mature temperate woodlands are commonly dominated by ectomycorrhizal trees, whereas understory plants predominantly form arbuscular mycorrhizal associations. Due to differences in plant-fungus compatibility between canopy and ground layer vegetation the 'mycorrhizal mediation hypothesis' predicts that herbaceous plant establishment may be limited by a lack of suitable mycorrhizal fungal inoculum. We examined plant species data for 103 woodlands across Great Britain recorded in 1971 and in 2000 to test whether herbaceous plant species richness was related to the proportion of arbuscular mycorrhizal woody plants. We compared the effect of mycorrhizal type with other important drivers of woodland plant species richness. We found a positive effect of the relative abundance of arbuscular mycorrhizal woody plants on herbaceous plant species richness. The size of the observed effect was smaller than that of pH. Moreover, the effect persisted over time, despite many woodlands undergoing marked successional change and increased understorey shading. This work supports the mycorrhizal mediation hypothesis in British woodlands and suggests that increased abundance of arbuscular mycorrhizal woody plants is associated with greater understory plant species richness.

The impact of the decomposition process of shallow graves on soil mite abundance.

Burial of a cadaver results in a slower decomposition rate, due to more stable below-ground temperatures and restricted access to necrophagous insects. In such circumstances, analysis of the soil mesofauna, with emphasis on mites (Acari) may be more valuable in time-of-death estimations. The production of volatile organic compounds of cadaveric decay results in changes, especially in the soil pH, which in turn would affect the abundance and diversity of the associated mites. In general, the effects of decomposition and the consequently altered pH levels on the abundance of mites in shallow graves, as well as the effects of fluctuating above-ground environmental parameters (temperature, relative humidity, and precipitation) remain unknown. Here, we found that the decay of three pig cadavers buried in shallow graves (<30 cm below) caused a significant increase in the soil pH throughout decomposition, from neutral to alkaline. Cadaver decay attracted an abundance of mites: with 300 mites collected from the three pig cadavers compared to 129 from the control soil samples at the same depth. Mites rapidly became more abundant in cadaver-associated soils than in control soils after the fresh stage. Increasing soil pH had a positive impact on the abundance of mites in graves and there was a significant interaction between cadaver body temperature and soil pH. Above-ground fluctuations in temperature, relative humidity, and precipitation were found to have no significant direct effect on mite abundance in grave or control soils.

Assemblages of Acari in shallow burials: mites as markers of the burial environment, of the stage of decay and of body-cadaver regions.

The burial of a cadaver results in reduced arthropod activity and disruptions in colonisation patterns. Here, the distribution and diversity of mite taxa was studied across decomposition stages of shallowly buried pig carcasses (Sus scrofa domesticus). In total 300 mites (88 species) were collected from three pig shallow graves compared to 129 mites (46 species) from control (bare) soil samples at the same depth. A successional pattern of Acari higher taxa and families was observed, and species richness and biodiversity fluctuated throughout decomposition, whereas active decay showed the greatest biodiversity. Mesostigmata mites were the most abundant in 'cadaver soils' with a significant difference in the abundance of Parasitidae mites, whereas Oribatida mites (true soil mites) were the most abundant in control soils. Certain mite species were significantly associated with decay stages: Cornigamasus lunaris with 'bloated', Gamasodes spiniger with 'active', Eugamasus sp. and Lorryia reticulata with 'advanced', and Macrocheles matrius and Ramusella clavipectinata in 'dry'. Scheloribates laevigatus was a marker of bare soil at a shallow depth and Vulgoramasus remberti of buried decomposition, not specific to any decay stage. Analysis of mite assemblages associated with head, torso and posterior body showed that Parasitus evertsi and M. matrius are attracted to beneath the thighs, whereas L. reticulata to beneath the head. This study highlights the value of mites as indicator species of decomposition and its stages, confirming (1) a succession of Acari on buried remains and (2) species specificity to body regions.

Wild insect diversity increases inter-annual stability in global crop pollinator communities.

While an increasing number of studies indicate that the range, diversity and abundance of many wild pollinators has declined, the global area of pollinator-dependent crops has significantly increased over the last few decades. Crop pollination studies to date have mainly focused on either identifying different guilds pollinating various crops, or on factors driving spatial changes and turnover observed in these communities. The mechanisms driving temporal stability for ecosystem functioning and services, however, remain poorly understood. Our study quantifies temporal variability observed in crop pollinators in 21 different crops across multiple years at a global scale. Using data from 43 studies from six continents, we show that (i) higher pollinator diversity confers greater inter-annual stability in pollinator communities, (ii) temporal variation observed in pollinator abundance is primarily driven by the three-most dominant species, and (iii) crops in tropical regions demonstrate higher inter-annual variability in pollinator species richness than crops in temperate regions. We highlight the importance of recognizing wild pollinator diversity in agricultural landscapes to stabilize pollinator persistence across years to protect both biodiversity and crop pollination services. Short-term agricultural management practices aimed at dominant species for stabilizing pollination services need to be considered alongside longer term conservation goals focussed on maintaining and facilitating biodiversity to confer ecological stability.

Shifts in Ectomycorrhizal Fungal Communities and Exploration Types Relate to the Environment and Fine-Root Traits Across Interior Douglas-Fir Forests of Western Canada.

Large-scale studies that examine the responses of ectomycorrhizal fungi across biogeographic gradients are necessary to assess their role in mediating current and predicted future alterations in forest ecosystem processes. We assessed the extent of environmental filtering on interior Douglas-fir (Pseudotsuga menziesii var. glauca (Beissn.) Franco) ectomycorrhizal fungal communities across regional gradients in precipitation, temperature, and soil fertility in interior Douglas-fir dominated forests of western Canada. We also examined relationships between fine-root traits and mycorrhizal fungal exploration types by combining root and fungal trait measurements with next-generation sequencing. Temperature, precipitation, and soil C:N ratio affected fungal community dissimilarity and exploration type abundance but had no effect on α-diversity. Fungi with rhizomorphs (e.g., Piloderma sp.) or proteolytic abilities (e.g., Cortinarius sp.) dominated communities in warmer and less fertile environments. Ascomycetes (e.g., Cenococcum geophilum) or shorter distance explorers, which potentially cost the plant less C, were favored in colder/drier climates where soils were richer in total nitrogen. Environmental filtering of ectomycorrhizal fungal communities is potentially related to co-evolutionary history between Douglas-fir populations and fungal symbionts, suggesting success of interior Douglas-fir as climate changes may be dependent on maintaining strong associations with local communities of mycorrhizal fungi. No evidence for a link between root and fungal resource foraging strategies was found at the regional scale. This lack of evidence further supports the need for a mycorrhizal symbiosis framework that is independent of root trait frameworks, to aid in understanding belowground plant uptake strategies across environments.

Below-ground biotic interactions moderated the postglacial range dynamics of trees.

Tree range shifts during geohistorical global change events provide a useful real-world model for how future changes in forest biomes may proceed. In North America, during the last deglaciation, the distributions of tree taxa varied significantly as regards the rate and direction of their responses for reasons that remain unclear. Local-scale processes such as establishment, growth, and resilience to environmental stress ultimately influence range dynamics. Despite the fact that interactions between trees and soil biota are known to influence local-scale processes profoundly, evidence linking below-ground interactions to distribution dynamics remains scarce. We evaluated climate velocity and plant traits related to dispersal, environmental tolerance and below-ground symbioses, as potential predictors of the geohistorical rates of expansion and contraction of the core distributions of tree genera between 16 and 7 ka bp. The receptivity of host genera towards ectomycorrhizal fungi was strongly supported as a positive predictor of poleward rates of distribution expansion, and seed mass was supported as a negative predictor. Climate velocity gained support as a positive predictor of rates of distribution contraction, but not expansion. Our findings indicate that understanding how tree distributions, and thus forest ecosystems, respond to climate change requires the simultaneous consideration of traits, biotic interactions and abiotic forcing.

The paleosymbiosis hypothesis: host plants can be colonised by root symbionts that have been inactive for centuries to millenia.

Paleoecologists have speculated that post-glacial migration of tree species could have been facilitated by mycorrhizal symbionts surviving glaciation as resistant propagules belowground. The general premise of this idea, which we call the 'paleosymbiosis hypothesis', is that host plants can access and be colonised by fungal root symbionts that have been inactive for millennia. Here, we explore the plausibility of this hypothesis by synthesising relevant findings from a diverse literature. For example, the paleoecology literature provided evidence of modern roots penetrating paleosols containing ancient (>6000 years) fungal propagules, though these were of unknown condition. With respect to propagule longevity, the available evidence is of mixed quality, but includes convincing examples consistent with the paleosymbiosis hypothesis (i.e. >1000 years viable propagules). We describe symbiont traits and environmental conditions that should favour the development and preservation of an ancient propagule bank, and discuss the implications for our understanding of soil symbiont diversity and ecosystem functioning. We conclude that the paleosymbiosis hypothesis is plausible in locations where propagule deposition and preservation conditions are favourable (e.g. permafrost regions). We encourage future belowground research to consider and explore the potential temporal origins of root symbioses.

Exploring the symbiont diversity of ancient western redcedars: arbuscular mycorrhizal fungi of long-lived hosts.

Arbuscular mycorrhizal fungi (AMF) are globally distributed, monophyletic root symbionts with ancient origins. Their contribution to carbon cycling and nutrient dynamics is ecologically important, given their obligate association with over 70% of vascular plant species. Current understanding of AMF species richness and community structure is based primarily on studies of grasses, herbs and agricultural crops, typically in disturbed environments. Few studies have considered AMF interactions with long-lived woody perennial species in undisturbed ecosystems. Here we examined AMF communities associated with roots and soils of young, mature and old western redcedar (Thuja plicata) at two sites in the old-growth temperate rainforests of British Columbia. Due to the unique biology of AMF, community richness and structure were assessed using a conservative, clade-based approach. We found 91 AMF OTUs across all samples, with significantly greater AMF richness in the southern site, but no differences in richness along the host chronosequence at either site. All host age classes harboured AMF communities that were overdispersed (more different to each other than expected by chance), with young tree communities most resembling old tree communities. A comparison with similar clade richness data obtained from the literature indicates that western redcedar AMF communities are as rich as those of grasses, tropical trees and palms. Our examination of undisturbed temperate old-growth rainforests suggests that priority effects, rather than succession, are an important aspect of AMF community assembly in this ecosystem.

Transfer of 13 C between paired Douglas-fir seedlings reveals plant kinship effects and uptake of exudates by ectomycorrhizas.

Processes governing the fixation, partitioning, and mineralization of carbon in soils are under increasing scrutiny as we develop a more comprehensive understanding of global carbon cycling. Here we examined fixation by Douglas-fir seedlings and transfer to associated ectomycorrhizal fungi, soil microbes, and full-sibling or nonsibling neighbouring seedlings. Stable isotope probing with 99% 13 C-CO2 was applied to trace 13 C-labelled photosynthate throughout plants, fungi, and soil microbes in an experiment designed to assess the effect of relatedness on 13 C transfer between plant pairs. The fixation and transfer of the 13 C label to plant, fungal, and soil microbial tissue was examined in biomass and phospholipid fatty acids. After a 6 d chase period, c. 26.8% of the 13 C remaining in the system was translocated below ground. Enrichment was proportionally greatest in ectomycorrhizal biomass. The presence of mesh barriers (0.5 or 35 µm) between seedlings did not restrict 13 C transfer. Fungi were the primary recipients of 13 C-labelled photosynthate throughout the system, representing 60-70% of total 13 C-enriched phospholipids. Full-sibling pairs exhibited significantly greater 13 C transfer to recipient roots in two of four Douglas-fir families, representing three- and fourfold increases (+ c. 4 µg excess 13 C) compared with nonsibling pairs. The existence of a root/mycorrhizal exudation-hyphal uptake pathway was supported.

Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities.

Adaptive behaviour of plants, including rapid changes in physiology, gene regulation and defence response, can be altered when linked to neighbouring plants by a mycorrhizal network (MN). Mechanisms underlying the behavioural changes include mycorrhizal fungal colonization by the MN or interplant communication via transfer of nutrients, defence signals or allelochemicals. We focus this review on our new findings in ectomycorrhizal ecosystems, and also review recent advances in arbuscular mycorrhizal systems. We have found that the behavioural changes in ectomycorrhizal plants depend on environmental cues, the identity of the plant neighbour and the characteristics of the MN. The hierarchical integration of this phenomenon with other biological networks at broader scales in forest ecosystems, and the consequences we have observed when it is interrupted, indicate that underground 'tree talk' is a foundational process in the complex adaptive nature of forest ecosystems.

Navigating the labyrinth: a guide to sequence-based, community ecology of arbuscular mycorrhizal fungi.

Data generated from next generation sequencing (NGS) will soon comprise the majority of information about arbuscular mycorrhizal fungal (AMF) communities. Although these approaches give deeper insight, analysing NGS data involves decisions that can significantly affect results and conclusions. This is particularly true for AMF community studies, because much remains to be known about their basic biology and genetics. During a workshop in 2013, representatives from seven research groups using NGS for AMF community ecology gathered to discuss common challenges and directions for future research. Our goal was to improve the quality and accessibility of NGS data for the AMF research community. Discussions spanned sampling design, sample preservation, sequencing, bioinformatics and data archiving. With concrete examples we demonstrated how different approaches can significantly alter analysis outcomes. Failure to consider the consequences of these decisions may compound bias introduced at each step along the workflow. The products of these discussions have been summarized in this paper in order to serve as a guide for any researcher undertaking NGS sequencing of AMF communities.

Local adaptation in migrated interior Douglas-fir seedlings is mediated by ectomycorrhizas and other soil factors.

Separating edaphic impacts on tree distributions from those of climate and geography is notoriously difficult. Aboveground and belowground factors play important roles, and determining their relative contribution to tree success will greatly assist in refining predictive models and forestry strategies in a changing climate. In a common glasshouse, seedlings of interior Douglas-fir (Pseudotsuga menziesii var. glauca) from multiple populations were grown in multiple forest soils. Fungicide was applied to half of the seedlings to separate soil fungal and nonfungal impacts on seedling performance. Soils of varying geographic and climatic distance from seed origin were compared, using a transfer function approach. Seedling height and biomass were optimized following seed transfer into drier soils, whereas survival was optimized when elevation transfer was minimised. Fungicide application reduced ectomycorrhizal root colonization by c. 50%, with treated seedlings exhibiting greater survival but reduced biomass. Local adaptation of Douglas-fir populations to soils was mediated by soil fungi to some extent in 56% of soil origin by response variable combinations. Mediation by edaphic factors in general occurred in 81% of combinations. Soil biota, hitherto unaccounted for in climate models, interacts with biogeography to influence plant ranges in a changing climate.

Host and habitat filtering in seedling root-associated fungal communities: taxonomic and functional diversity are altered in 'novel' soils.

Climatic and land use changes have significant consequences for the distribution of tree species, both through natural dispersal processes and following management prescriptions. Responses to these changes will be expressed most strongly in seedlings near current species range boundaries. In northern temperate forest ecosystems, where changes are already being observed, ectomycorrhizal fungi contribute significantly to successful tree establishment. We hypothesised that communities of fungal symbionts might therefore play a role in facilitating, or limiting, host seedling range expansion. To test this hypothesis, ectomycorrhizal communities of interior Douglas-fir and interior lodgepole pine seedlings were analysed in a common greenhouse environment following growth in five soils collected along an ecosystem gradient. Currently, Douglas-fir's natural distribution encompasses three of the five soils, whereas lodgepole pine's extends much further north. Host filtering was evident amongst the 29 fungal species encountered: 7 were shared, 9 exclusive to Douglas-fir and 13 exclusive to lodgepole pine. Seedlings of both host species formed symbioses with each soil fungal community, thus Douglas-fir did so even where those soils came from outside its current distribution. However, these latter communities displayed significant taxonomic and functional differences to those found within the host distribution, indicative of habitat filtering. In contrast, lodgepole pine fungal communities displayed high functional similarity across the soil gradient. Taxonomic and/or functional shifts in Douglas-fir fungal communities may prove ecologically significant during the predicted northward migration of this species; especially in combination with changes in climate and management operations, such as seed transfer across geographical regions for forestry purposes.

Spatial analysis of ectomycorrhizal fungi reveals that root tip communities are structured by competitive interactions.

Microbial ecology has made large advances over the last decade, mostly because of improvements in molecular analysis techniques that have enabled the detection and identification of progressively larger numbers of microbial species. However, determining the ecological patterns and processes taking place in communities of microbes remains a significant challenge. Are communities randomly assembled through dispersal and priority effects, or do species interact with each other leading to positive and negative associations? For mycorrhizal fungi, evidence is accumulating that stochastic and competitive interactions between species may both have a role in shaping community structure. Could the methodological approach, which is often incidence based, impact the outcomes detected? Here, we applied an incidence-based Terminal Restriction Fragment Length Polymorphism (T-RFLP) database approach to examine species diversity and ecological interactions within a community of ectomycorrhizal (ECM) fungi. Co-occurrence analysis revealed that the ECM community colonizing root tips was strongly structured by competitive interactions, or ecological processes generating a similar spatial pattern, rather than neutral processes. Analysis of ß-diversity indicated that community structure was significantly more similar (spatially autocorrelated) at distances equal to or <3.41 m. The eight most frequently encountered species in the root tip community of ECM fungi displayed significant competitive interactions with at least one other species, showing that the incidence-based approach was capable of detecting this sort of ecological information.

Spatial and temporal ecology of Scots pine ectomycorrhizas.

Spatial analysis was used to explore the distribution of individual species in an ectomycorrhizal (ECM) fungal community to address: whether mycorrhizas of individual ECM fungal species were patchily distributed, and at what scale; and what the causes of this patchiness might be. Ectomycorrhizas were extracted from spatially explicit samples of the surface organic horizons of a pine plantation. The number of mycorrhizas of each ECM fungal species was recorded using morphotyping combined with internal transcribed spacer (ITS) sequencing. Semivariograms, kriging and cluster analyses were used to determine both the extent and scale of spatial autocorrelation in species abundances, potential interactions between species, and change over time. The mycorrhizas of some, but not all, ECM fungal species were patchily distributed and the size of patches differed between species. The relative abundance of individual ECM fungal species and the position of patches of ectomycorrhizas changed between years. Spatial and temporal analysis revealed a dynamic ECM fungal community with many interspecific interactions taking place, despite the homogeneity of the host community. The spatial pattern of mycorrhizas was influenced by the underlying distribution of fine roots, but local root density was in turn influenced by the presence of specific fungal species.