Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: A trait-based predictive framework

Anthropogenic nitrogen (N) deposition is exposing plants and their arbuscular mycorrhizal fungi (AMFs) to elevated N availability, often leading to shifts in communities of AMF. However, physiological trade-offs among AMF taxa in their response to N enrichment vs the ability to acquire other soil nutrients could have negative effects on plant and ecosystem productivity. It follows that information on the functional traits of AMF taxa can be used to generate predictions of their potential role in mediating ecosystem responses to N enrichment. Arbuscular mycorrhizal fungi taxa that produce extensive networks of external hyphae should forage for N and phosphorus (P) more effectively, but these services incur greater carbon (C) costs to the plant. If N enrichment ameliorates plant nutrient limitation, then plants may reduce C available for AMF, which in turn could eliminate AMF taxa with large extensive external hyphae from the soil community. As a result, the remaining AMF taxa may confer less P benefit to their host plants. Using a synthesis of data from the literature, we found that the ability of a taxon to persist in the face of increasing soil N availability was particularly high in isolates from the genus Glomus, but especially low among the Gigasporaceae. Across AMF genera, our data support the prediction that AMF with a tolerance for high soil N may confer a lower P benefit to their host plant. Relationships between high N tolerance and production of external hyphae were mixed. Synthesis. If the relationship between N tolerance and plant P benefit is widespread, then shifts in arbuscular mycorrhizal fungi communities associated with N deposition could have negative consequences for the ability of plants to acquire P and possibly other nutrients via a mycorrhizal pathway. Based on this relationship, we predict that arbuscular mycorrhizal fungi responses could constrain net primary productivity in P-limited ecosystems exposed to N enrichment. This prediction could be tested in future empirical and modelling studies

Diversity Effects on Productivity Are Stronger within than between Trophic Groups in the Arbuscular Mycorrhizal Symbiosis

The diversity of plants and arbuscular mycorrhizal fungi (AMF) has been experimentally shown to alter plant and AMF productivity. However, little is known about how plant and AMF diversity interact to shape their respective productivity.We co-manipulated the diversity of both AMF and plant communities in two greenhouse studies to determine whether the productivity of each trophic group is mainly influenced by plant or AMF diversity, respectively, and whether there is any interaction between plant and fungal diversity. In both experiments we compared the productivity of three different plant species monocultures, or their respective 3-species mixtures. Similarly, in both studies these plant treatments were crossed with an AMF diversity gradient that ranged from zero (non-mycorrhizal controls) to a maximum of three and five taxonomically distinct AMF taxa, respectively. We found that within both trophic groups productivity was significantly influenced by taxon identity, and increased with taxon richness. These main effects of AMF and plant diversity on their respective productivities did not depend on each other, even though we detected significant individual taxon effects across trophic groups.Our results indicate that similar ecological processes regulate diversity-productivity relationships within trophic groups. However, productivity-diversity relationships are not necessarily correlated across interacting trophic levels, leading to asymmetries and possible biotic feedbacks. Thus, biotic interactions within and across trophic groups should be considered in predictive models of community assembly

The Influence of Different Stresses on Glomalin Levels in an Arbuscular Mycorrhizal Fungus—Salinity Increases Glomalin Content

Glomalin is a glycoprotein produced by arbuscular mycorrhizal (AM) fungi, and the soil fraction containing glomalin is correlated with soil aggregation. Thus, factors potentially influencing glomalin production could be of relevance for this ecosystem process and for understanding AM fungal physiology. Previous work indicated that glomalin production in AM fungi may be a stress response, or related to suboptimal mycelium growth. We show here that environmental stress can enhance glomalin production in the mycelium of the AM fungus Glomus intraradices. We applied NaCl and glycerol in different intensities to the medium in which the fungus was grown in vitro, causing salinity stress and osmotic stress, respectively. As a third stress type, we simulated grazing on the extraradical hyphae of the fungus by mechanically injuring the mycelium by clipping. NaCl caused a strong increase, while the clipping treatment led to a marginally significant increase in glomalin production. Even though salinity stress includes osmotic stress, we found substantially different responses in glomalin production due to the NaCl and the glycerol treatment, as glycerol addition did not cause any response. Thus, our results indicate that glomalin is involved in inducible stress responses in AM fungi for salinity, and possibly grazing stress

Techniques for Arbuscular Mycorrhiza Inoculum Reduction

It is well established that arbuscular mycorrhizal (AM) fungi can play a significant role in sustainable crop production and environmental conservation. With the increasing awareness of the ecological significance of mycorrhizas and their diversity, research needs to be directed away from simple records of their occurrence or casual speculation of their function (Smith and Read 1997). Rather, the need is for empirical studies and investigations of the quantitative aspects of the distribution of different types and their contribution to the function of ecosystems. There is no such thing as a fungal effect or a plant effect, but there is an interaction between both symbionts. This results from the AM fungi and plant community size and structure, soil and climatic conditions, and the interplay between all these factors (Kahiluoto et al. 2000). Consequently, it is readily understood that it is the problems associated with methodology that limit our understanding of the functioning and effects of AM fungi within field communities. Given the ubiquous presence of AM fungi, a major constraint to the evaluation of the activity of AM colonisation has been the need to account for the indigenous soil native inoculum. This has to be controlled (i.e. reduced or eliminated) if we are to obtain a true control treatment for analysis of arbuscular mycorrhizas in natural substrates. There are various procedures possible for achieving such an objective, and the purpose of this chapter is to provide details of a number of techniques and present some evaluation of their advantages and disadvantages. Although there have been a large number of experiments to investigated the effectiveness of different sterilization procedures for reducing pathogenic soil fungi, little information is available on their impact on beneficial organisms such as AM fungi. Furthermore, some of the techniques have been shown to affect physical and chemical soil characteristics as well as eliminate soil microorganisms that can interfere with the development of mycorrhizas, and this creates difficulties in the interpretation of results simply in terms of possible mycorrhizal activity. An important subject is the differentiation of methods that involve sterilization from those focussed on indigenous inoculum reduction. Soil sterilization aims to destroy or eliminate microbial cells while maintaining the existing chemical and physical characteristics of the soil (Wolf and Skipper 1994). Consequently, it is often used for experiments focussed on specific AM fungi, or to establish a negative control in some other types of study. In contrast, the purpose of inoculum reduction techniques is to create a perturbation that will interfere with mycorrhizal formation, although not necessarily eliminating any component group within the inoculum. Such an approach allows the establishment of different degrees of mycorrhizal formation between treatments and the study of relative effects. Frequently the basic techniques used to achieve complete sterilization or just an inoculum reduction may be similar but the desired outcome is accomplished by adjustments of the dosage or intensity of the treatment. The ultimate choice of methodology for establishing an adequate non-mycorrhizal control depends on the design of the particular experiments, the facilities available and the amount of soil requiring treatment

Evidence for Enhanced Mutualism Hypothesis: Solidago canadensis Plants from Regular Soils Perform Better

The important roles of plant-soil microbe interactions have been documented in exotic plant invasion, but we know very little about how soil mutualists enhance this process (i.e. enhanced mutualism hypothesis). To test this hypothesis we conducted two greenhouse experiments with Solidago canadensis (hereafter Solidago), an invasive forb from North America, and Stipa bungeana (hereafter Stipa), a native Chinese grass. In a germination experiment, we found soil microbes from the rhizospheres of Solidago and Stipa exhibited much stronger facilitative effects on emergence of Solidago than that of Stipa. In a growth and competition experiment, we found that soil microbes strongly facilitated Solidago to outgrow Stipa, and greatly increased the competitive effects of Solidago on Stipa but decreased the competitive effects of Stipa on Solidago. These findings from two experiments suggest that in situ soil microbes enhance the recruitment potential of Solidago and its ability to outcompete native plants, thereby providing strong evidence for the enhanced mutualism hypothesis. On the other hand, to some extent this outperformance of Solidago in the presence of soil microbes seems to be unbeneficial to control its rapid expansion, particularly in some ranges where this enhanced mutualism dominates over other mechanisms

Plant–soil feedback of native and range-expanding plant species is insensitive to temperature

Temperature change affects many aboveground and belowground ecosystem processes. Here we investigate the effect of a 5°C temperature increase on plant–soil feedback. We compare plant species from a temperate climate region with immigrant plants that originate from warmer regions and have recently shifted their range polewards. We tested whether the magnitude of plant–soil feedback is affected by ambient temperature and whether the effect of temperature differs between these groups of plant species. Six European/Eurasian plant species that recently colonized the Netherlands (non-natives), and six related species (natives) from the Netherlands were selected. Plant–soil feedback of these species was determined by comparing performance in conspecific and heterospecific soils. In order to test the effect of temperature on these plant–soil feedback interactions, the experiments were performed at two greenhouse temperatures of 20/15°C and 25/20°C, respectively. Inoculation with unconditioned soil had the same effect on natives and non-natives. However, the effect of conspecific conditioned soil was negative compared to heterospecific soil for natives, but was positive for non-natives. In both cases, plant–soil interactions were not affected by temperature. Therefore, we conclude that the temperature component of climate change does not affect the direction, or strength of plant–soil feedback, neither for native nor for non-native plant species. However, as the non-natives have a more positive soil feedback than natives, climate warming may introduce new plant species in temperate regions that have less soil-borne control of abundance

Arbuscular mycorrhizal colonisation of roots of grass species differing in invasiveness

Recent research indicates that the soil microbial community, particularly arbuscular mycorrhizal fungi (AMF), can influence plant invasion in several ways. We tested if 1) invasive species are colonised by AMF to a lower degree than resident native species, and 2) AMF colonisation of native plants is lower in a community inhabited by an invasive species than in an uninvaded resident community. The two tests were run in semiarid temperate grasslands on grass (Poaceae) species, and the frequency and intensity of mycorrhizal colonisation, and the proportion of arbuscules and vesicles in plant roots have been measured. In the first test, grasses representing three classes of invasiveness were included: invasive species, resident species becoming abundant upon disturbance, and non-invasive native species. Each class contained one C3 and one C4 species. The AMF colonisation of the invasive Calamagrostis epigejos and Cynodon dactylon was consistently lower than that of the non-invasive native Chrysopogon gryllus and Bromus inermis, and contained fewer arbuscules than the post-disturbance dominant resident grasses Bothriochloa ischaemum and Brachypodium pinnatum. The C3 and C4 grasses behaved alike despite their displaced phenologies in these habitats. The second test compared AMF colonisation for sand grassland dominant grasses Festuca vaginata and Stipa borysthenica in stands invaded by either C. epigejos or C. dactylon, and in the uninvaded natural community. Resident grasses showed lower degree of AMF colonisation in the invaded stand compared to the uninvaded natural community with F. vaginata responding so to both invaders, while S. borysthenica responding to C. dactylon only. These results indicate that invasive grasses supposedly less reliant on AMF symbionts have the capacity of altering the soil mycorrhizal community in such a way that resident native species can establish a considerably reduced extent of the beneficial AMF associations, hence their growth, reproduction and ultimately abundance may decline. Accumulating evidence suggests that such indirect influences of invasive alien plants on resident native species mediated by AMF or other members of the soil biota is probably more the rule than the exception

Can Arbuscular Mycorrhizal Fungi Reduce the Growth of Agricultural Weeds?

BACKGROUND: Arbuscular mycorrhizal fungi (AMF) are known for their beneficial effects on plants. However, there is increasing evidence that some ruderal plants, including several agricultural weeds, respond negatively to AMF colonization. Here, we investigated the effect of AMF on the growth of individual weed species and on weed-crop interactions. METHODOLOGY/PRINCIPAL FINDINGS: First, under controlled glasshouse conditions, we screened growth responses of nine weed species and three crops to a widespread AMF, Glomus intraradices. None of the weeds screened showed a significant positive mycorrhizal growth response and four weed species were significantly reduced by the AMF (growth responses between -22 and -35%). In a subsequent experiment, we selected three of the negatively responding weed species--Echinochloa crus-galli, Setaria viridis and Solanum nigrum--and analyzed their responses to a combination of three AMF (Glomus intraradices, Glomus mosseae and Glomus claroideum). Finally, we tested whether the presence of a crop (maize) enhanced the suppressive effect of AMF on weeds. We found that the growth of the three selected weed species was also reduced by a combination of AMF and that the presence of maize amplified the negative effect of AMF on the growth of E. crus-galli. CONCLUSIONS/SIGNIFICANCE: Our results show that AMF can negatively influence the growth of some weed species indicating that AMF have the potential to act as determinants of weed community structure. Furthermore, mycorrhizal weed growth reductions can be amplified in the presence of a crop. Previous studies have shown that AMF provide a number of beneficial ecosystem services. Taken together with our current results, the maintenance and promotion of AMF activity may thereby contribute to sustainable management of agroecosystems. However, in order to further the practical and ecological relevance of our findings, additional experiments should be performed under field conditions

Community Compensatory Trend Prevails from Tropical to Temperate Forest

Community compensatory trend (CCT) is thought to facilitate persistence of rare species and thus stabilize species composition in tropical forests. However, whether CCT acts over broad geographical ranges is still in question. In this study, we tested for the presence of negative density dependence (NDD) and CCT in three forests along a tropical-temperate gradient. Inventory data were collected from forest communities located in three different latitudinal zones in China. Two widely used methods were used to test for NDD at the community level. The first method considered relationships between the relative abundance ratio and adult abundance. The second method emphasized the effect of adult abundance on abundance of established younger trees. Evidence for NDD acting on different growth forms was tested by using the first method, and the presence of CCT was tested by checking whether adult abundance of rare species affected that of established younger trees less than did abundance of common species. Both analyses indicated that NDD existed in seedling, sapling and pole stages in all three plant communities and that this effect increased with latitude. However, the extent of NDD varied among understory, midstory and canopy trees in the three communities along the gradient. Additionally, despite evidence of NDD for almost all common species, only a portion of rare species showed NDD, supporting the action of CCT in all three communities. So, we conclude that NDD and CCT prevail in the three recruitment stages of the tree communities studied; rare species achieve relative advantage through CCT and thus persist in these communities; CCT clearly facilitates newly established species and maintains tree diversity within communities across our latitudinal gradient

Agronomic Management of Indigenous Mycorrhizas

Many of the advantages conferred to plants by arbuscular mycorrhiza (AM) are associated to the ability of AM plants to explore a greater volume of soil through the extraradical mycelium. Sieverding (1991) estimates that for each centimetre of colonized root there is an increase of 15 cm3 on the volume of soil explored, this value can increase to 200 cm3 depending on the circumstances. Due to the enhancement of the volume of soil explored and the ability of the extraradical mycelium to absorb and translocate nutrients to the plant, one of the most obvious and important advantages resulting from mycorrhization is the uptake of nutrients. Among of which the ones that have immobilized forms in soil, such as P, assume particular significance. Besides this, many other benefits are recognized for AM plants (Gupta et al, 2000): water stress alleviation (Augé, 2004; Cho et al, 2006), protection from root pathogens (Graham, 2001), tolerance to toxic heavy metals and phytoremediation (Audet and Charest, 2006; Göhre and Paszkowski, 2006), tolerance to adverse conditions such as very high or low temperature, high salinity (Sannazzaro et al, 2006), high or low pH (Yano and Takaki, 2005) or better performance during transplantation shock (Subhan et al, 1998). The extraradical hyphae also stabilize soil aggregates by both enmeshing soil particles (Miller e Jastrow, 1992) and producing a glycoprotein, golmalin, which may act as a glue-like substance to adhere soil particles together (Wright and Upadhyaya, 1998). Despite the ubiquous distribution of mycorrhizal fungi (Smith and Read, 2000) and only a relative specificity between host plants and fungal isolates (McGonigle and Fitter, 1990), the obligate nature of the symbiosis implies the establishment of a plant propagation system, either under greenhouse conditions or in vitro laboratory propagation. These techniques result in high inoculum production costs, which still remains a serious problem since they are not competitive with production costs of phosphorus fertilizer. Even if farmers understand the significance of sustainable agricultural systems, the reduction of phosphorus inputs by using AM fungal inocula alone cannot be justified except, perhaps, in the case of high value crops (Saioto and Marumoto, 2002). Nurseries, high income horticulture farmers and no-agricultural application such as rehabilitation of degraded or devegetated landscapes are examples of areas where the use of commercial inoculum is current. Another serious problem is quality of commercial available products concerning guarantee of phatogene free content, storage conditions, most effective application methods and what types to use. Besides the information provided by suppliers about its inoculum can be deceiving, as from the usually referred total counts, only a fraction may be effective for a particular plant or in specific soil conditions. Gianinazzi and Vosátka (2004) assume that progress should be made towards registration procedures that stimulate the development of the mycorrhizal industry. Some on-farm inoculum production and application methods have been studied, allowing farmers to produce locally adapted isolates and generate a taxonomically diverse inoculum (Mohandas et al, 2004; Douds et al, 2005). However the inocula produced this way are not readily processed for mechanical application to the fields, being an obstacle to the utilization in large scale agriculture, especially row crops, moreover it would represent an additional mechanical operation with the corresponding economic and soil compaction costs. It is well recognized that inoculation of AM fungi has a potential significance in not only sustainable crop production, but also environmental conservation. However, the status quo of inoculation is far from practical technology that can be widely used in the field. Together a further basic understanding of the biology and diversity of AM fungi is needed (Abbott at al, 1995; Saito and Marumoto, 2002). Advances in ecology during the past decade have led to a much more detailed understanding of the potential negative consequences of species introductions and the potential for negative ecological consequences of invasions by mycorrhizal fungi is poorly understood. Schwartz et al, (2006) recommend that a careful assessment documenting the need for inoculation, and the likelihood of success, should be conducted prior to inoculation because inoculations are not universally beneficial. Agricultural practices such as crop rotation, tillage, weed control and fertilizer apllication all produce changes in the chemical, physical and biological soil variables and affect the ecological niches available for occupancy by the soil biota, influencing in different ways the symbiosis performance and consequently the inoculum development, shaping changes and upset balance of native populations. The molecular biology tools developed in the latest years have been very important for our perception of these changes, ensuing awareness of management choice implications in AM development. In this context, for extensive farming systems and regarding environmental and economic costs, the identification of agronomic management practices that allow controlled manipulation of the fungal community and capitalization of AM mutualistic effect making use of local inoculum, seem to be a wise option for mycorrhiza promotion and development of sustainable crop production