Cameron Wagg

Soil biodiversity and soil community composition determine ecosystem multifunctionality

Significance Biological diversity is the foundation for the maintenance of ecosystems. Consequently it is thought that anthropogenic activities that reduce the diversity in ecosystems threaten ecosystem performance. A large proportion of the biodiversity within terrestrial ecosystems is hidden below ground in soils, and the impact of altering its diversity and composition on the performance of ecosystems is still poorly understood. Using a novel experimental system to alter levels of soil biodiversity and community composition, we found that reductions in the abundance and presence of soil organisms results in the decline of multiple ecosystem functions, including plant diversity and nutrient cycling and retention. This suggests that below-ground biodiversity is a key resource for maintaining the functioning of ecosystems. Biodiversity loss has become a global concern as evidence accumulates that it will negatively affect ecosystem services on which society depends. So far, most studies have focused on the ecological consequences of above-ground biodiversity loss; yet a large part of Earth’s biodiversity is literally hidden below ground. Whether reductions of biodiversity in soil communities below ground have consequences for the overall performance of an ecosystem remains unresolved. It is important to investigate this in view of recent observations that soil biodiversity is declining and that soil communities are changing upon land use intensification. We established soil communities differing in composition and diversity and tested their impact on eight ecosystem functions in model grassland communities. We show that soil biodiversity loss and simplification of soil community composition impair multiple ecosystem functions, including plant diversity, decomposition, nutrient retention, and nutrient cycling. The average response of all measured ecosystem functions (ecosystem multifunctionality) exhibited a strong positive linear relationship to indicators of soil biodiversity, suggesting that soil community composition is a key factor in regulating ecosystem functioning. Our results indicate that changes in soil communities and the loss of soil biodiversity threaten ecosystem multifunctionality and sustainability.

Belowground biodiversity effects of plant symbionts support aboveground productivity

Soil microbes play key roles in ecosystems, yet the impact of their diversity on plant communities is still poorly understood. Here we demonstrate that the diversity of belowground plant-associated soil fungi promotes plant productivity and plant coexistence. Using additive partitioning of biodiversity effects developed in plant biodiversity studies, we demonstrate that this positive relationship can be driven by complementarity effects among soil fungi in one soil type and by a selection effect resulting from the fungal species that stimulated plant productivity the most in another soil type. Selection and complementarity effects among fungal species contributed to improving plant productivity up to 82% and 85%, respectively, above the average of the respective fungal species monocultures depending on the soil in which they were grown. These results also indicate that belowground diversity may act as insurance for maintaining plant productivity under differing environmental conditions.

Mycorrhizal fungal identity and diversity relaxes plant–plant competition

There is a great interest in ecology in understanding the role of soil microbial diversity for plant productivity and coexistence. Recent research has shown increases in species richness of mutualistic soil fungi, the arbuscular mycorrhizal fungi (AMF), to be related to increases in aboveground productivity of plant communities. However, the impact of AMF richness on plant-plant interactions has not been determined. Moreover, it is unknown whether species-rich AMF communities can act as insurance to maintain productivity in a fluctuating environment (e.g., upon changing soil conditions). We tested the impact of four different AMF taxa and of AMF diversity (no AMF, single AMF taxa, and all four together) on competitive interactions between the legume Trifolium pratense and the grass Lolium multiflorum grown under two different soil conditions of low and high sand content. We hypothesized that more diverse mutualistic interactions (e.g., when four AMF taxa are present) can ease competitive effects between plants, increase plant growth, and maintain plant productivity across different soil environments. We used quantitative PCR to verify that AMF taxa inoculated at the beginning of the experiment were still present at the end. The presence of AMF reduced the competitive inequality between the two plant species by reducing the growth suppression of the legume by the grass. High AMF richness enhanced the combined biomass production of the two plant species and the yield of the legume, particularly in the more productive soil with low sand content. In the less productive (high sand content) soil, the single most effective AMF had an equally beneficial effect on plant productivity as the mixture of four AMF. Since contributions of single AMF to plant productivity varied between both soils, higher AMF richness would be required to maintain plant productivity in heterogeneous environments. Overall this work shows that AMF diversity promotes plant productivity and that AMF diversity can act as insurance to sustain plant productivity under changing environmental conditions.

An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability

Soil organisms are an integral component of ecosystems, but their activities receive little recognition in agricultural management strategies. Here we synthesize the potential of soil organisms to enhance ecosystem service delivery and demonstrate that soil biodiversity promotes multiple ecosystem functions simultaneously (i.e., ecosystem multifunctionality). We apply the concept of ecological intensification to soils and we develop strategies for targeted exploitation of soil biological traits. We compile promising approaches to enhance agricultural sustainability through the promotion of soil biodiversity and targeted management of soil community composition. We present soil ecological engineering as a concept to generate human land-use systems, which can serve immediate human needs while minimizing environmental impacts.

Associations between microfungal endophytes and roots: do structural features indicate function?

Roots encounter a plethora of microorganisms in the soil environment that are either deleterious, neutral, or beneficial to plant growth. Root endophytic fungi are ubiquitous. These include dark septate endophytes whose role in plant growth and the maintenance of plant communities is largely unknown. The objectives of this review were to assess the structural features of the interactions between dark septate endophytic fungi and the roots of both angiopsperms and conifers, and to suggest avenues for further research. Several light microscopy studies of endophyte–root interactions have revealed a variety of structural features, depending on host species and plant growth conditions. In some cases, when fungal hyphae enter roots they cause cell breakdown, whereas in other situations there is little noticeable effect. In some tree species, associations with these endophytes may mimic ectomycorrhizas or ectendomycorrhizas. The few ultrastructural studies indicate that intracellular hyphae lack a host-derived p...

The co-occurrence of ectomycorrhizal, arbuscular mycorrhizal, and dark septate fungi in seedlings of four members of the Pinaceae

Although roots of species in the Pinaceae are usually colonized by ectomycorrhizal (EM) fungi, there are increasing reports of the presence of arbuscular mycorrhizal (AM) and dark septate endophytic (DSE) fungi in these species. The objective of this study was to determine the colonization patterns in seedlings of three Pinus (pine) species (Pinus banksiana, Pinus strobus, Pinus contorta) and Picea glauca x Picea engelmannii (hybrid spruce) grown in soil collected from a disturbed forest site. Seedlings of all three pine species and hybrid spruce became colonized by EM, AM, and DSE fungi. The dominant EM morphotype belonged to the E-strain category; limited colonization by a Tuber sp. was found on roots of Pinus strobus and an unknown morphotype (cf. Suillus–Rhizopogon group) with thick, cottony white mycelium was present on short roots of all species. The three fungal categories tended to occupy different niches in a single root system. No correlation was found between the percent root colonized by EM and percent colonization by either AM or DSE, although there was a positive correlation between percent root length colonized by AM and DSE. Hyphae and vesicles were the only AM intracellular structures found in roots of all species; arbuscules were not observed in any roots.

Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype

Lotus japonicus har1 mutants respond to inoculation with Mesorhizobium loti by forming an excessive number of nodules due to genetic lesions in the HAR1 autoregulatory receptor kinase gene. In order to expand the repertoire of mutants available for the genetic dissection of the root nodule symbiosis (RNS), a screen for suppressors of the L. japonicus har1-1 hypernodulation phenotype was performed. Of 150,000 M2 plants analyzed, 61 stable L. japonicus double-mutant lines were isolated. In the context of the har1-1 mutation, 26 mutant lines were unable to form RNS, whereas the remaining 35 mutant lines carried more subtle symbiotic phenotypes, either forming white ineffective nodules or showing reduced nodulation capacity. When challenged with Glomus intraradices, 18 of the 61 suppressor lines were unable to establish a symbiosis with this arbuscular mycorrhiza fungus. Using a combined approach of genetic mapping, targeting induced local lesions in genomics, and sequencing, all non-nodulating mutant lines were characterized and shown to represent new alleles of at least nine independent symbiotic loci. The class of mutants with reduced nodulation capacity was of particular interest because some of them may specify novel plant functions that regulate nodule development in L. japonicus. To facilitate mapping of the latter class of mutants, an introgression line, in which the har1-1 allele was introduced into a polymorphic background of L. japonicus ecotype MG20, was constructed.

Soil microbial diversity and agro-ecosystem functioning

Soil microbes represent the unseen majority of life on Earth and are essential for the functioning of terrestrial ecosystems as they catalyze unique and indispensable transformations in the biogeochemical cycles of the biosphere (Whitman et al. 1998; van der Heijden et al. 2008). The significance of soil microbial diversity for the functioning of agricultural and natural ecosystems is still poorly understood and soil microbial communities can be considered as a black box (Kennedy and Smith 1995; Cortois and de Deyn 2012). Unraveling what soil microbes are doing in this black box has been identified as one of the major research areas in science. An increasing number of studies demonstrate that agricultural practices, such as tree based intercropping (Lacombe et al. 2009; Bainard et al. 2012a, b), organic farming (Mäder et al. 2002; Bengtsson et al. 2005; Birkhofer et al. 2008; Verbruggen et al. 2010), reduced soil tillage (van Capelle et al. 2012), crop rotation (Altieri 1999; Cavagnaro and Martin 2011) and land use extensification (Postma-Blaauw et al. 2010; de Vries et al. 2012) have a positive impact on the abundance and richness of specific groups of soil organisms (e.g. arbuscular mycorrhizal fungi, earthworms) and on soil microbial diversity. Thus, by adapting farm management practices it is possible to favor recruitment of specific groups of soil organisms and enhance microbial diversity. As such, these findings make it possible to provide policy makers with recommendations on enhancing soil biodiversity in agricultural ecosystems. There are a number of mechanisms by which microbial diversity can support agro-ecosystem functioning and particular ecosystem functions such as plant productivity and decomposition. For instance, microbes can form “consortia” that enhance plant productivity (e.g. when different microbes provide different limiting resources to plants) or decomposition (e.g. when plant material is decomposed by specialized microbes with unique physiological properties that succeed each other). As a consequence, microbial diversity can promote ecosystem functioning. However, in other cases, the presence of key stone species (e.g. specific pathogens, nitrogen fixers) rather than diversity “per se” may determine agro-ecosystem functioning. Until now, it is still poorly understood, whether increased soil (microbial) diversity is beneficial for the functioning and sustainability of agricultural systems. Plant Soil (2013) 363:1–5 DOI 10.1007/s11104-012-1545-4

Soil microbial communities from an elevational cline differ in their effect on conifer seedling growth

Sub-alpine environments consist of altitudinal gradients associated with dramatic changes in plant growth and community composition, but the role of soil feedbacks and microbe interactions is largely unknown. Here, we examine the influence of the overall soil microbial community, with a focus on ectomycorrhizal and dark septate endophytic root colonizing fungi, from low, mid, and high elevations on the growth of Pinus contorta and Picea glauca × engelmannii. The influence of the soil microbial community was tested on seedlings from the same three elevations in order to determine ‘home’ versus ‘away’ effects on conspecifics of differing elevations. The low elevation soil was the most fertile and harbored a soil microbial community with an overall negative effect on seedling growth. In contrast, the high elevation soil was the least fertile and had a microbial community that enhanced seedling growth. However, only the soil microbial community in the highest elevation soil resulted in a stronger influence on the native P. contorta seedlings than seedlings originating from lower elevations. Despite the overall influence of the soil microbial community, ectomycorrhizal colonization was significantly correlated with P. glauca × engelmannii growth rates, but colonization by dark septate endophytes showed no relationship with seedling growth. The results provide evidence that plant—soil microbial community relationships are dependent on soil environment. Moreover, our results provide further support for the importance of soil microbes in facilitating seedling growth toward the edge of their elevational range.

Plant species richness and functional traits affect community stability after a flood event.

Climate change is expected to increase the frequency and magnitude of extreme weather events. It is therefore of major importance to identify the community attributes that confer stability in ecological communities during such events. In June 2013, a flood event affected a plant diversity experiment in Central Europe (Jena, Germany). We assessed the effects of plant species richness, functional diversity, flooding intensity and community means of functional traits on different measures of stability (resistance, resilience and raw biomass changes from pre-flood conditions). Surprisingly, plant species richness reduced community resistance in response to the flood. This was mostly because more diverse communities grew more immediately following the flood. Raw biomass increased over the previous year; this resulted in decreased absolute value measures of resistance. There was no clear response pattern for resilience. We found that functional traits drove these changes in raw biomass: communities with a high proportion of late-season, short-statured plants with dense, shallow roots and small leaves grew more following the flood. Late-growing species probably avoided the flood, whereas greater root length density might have allowed species to better access soil resources brought from the flood, thus growing more in the aftermath. We conclude that resource inputs following mild floods may favour the importance of traits related to resource acquisition and be less associated with flooding tolerance.