Interactions among mutualism,competition, and predation foster species coexistence in diverse communities

In natural systems, organisms are simultaneously engaged in mutualistic, competitive, and predatory interactions. Theory predicts that species persistence and community stability are feasible when the beneficial effects of mutualisms are balanced by density-dependent negative feedbacks. Enemy-mediated negative feedbacks can foster plant species coexistence in diverse communities, but empirical evidence remains mixed. Disparity between theoretical expectations and empirical results may arise from the effects of mutualistic mycorrhizal fungi. Here, we build a multiprey species/predator model combined with a bidirectional resource exchange system, which simulates mutualistic interactions between plants and fungi. To reach population persistence, (1) the per capita rate of increase of all plant population must exceed the sum of the negative per capita effects of predation, interspecific competition, and costs of mycorrhizal association, and (2) the per capita numerical response of enemies to mycorrhizal plants must exceed the magnitude of the per capita enemy rate of mortality. These conditions reflect the balance between regulation and facilitation in the system. Interactions between plant natural enemies and mycorrhizal fungi lead to shifts in the strength and direction of net mycorrhizal effects on plants over time, with common plant species deriving greater benefits from mycorrhizal associations than rare plant species.     

Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack

The roots of most land plants are colonised by mycorrhizal fungi that provide mineral nutrients in exchange for carbon. Here, we show that mycorrhizal mycelia can also act as a conduit for signalling between plants, acting as an early warning system for herbivore attack. Insect herbivory causes systemic changes in the production of plant volatiles, particularly methyl salicylate, making bean plants, Vicia faba, repellent to aphids but attractive to aphid enemies such as parasitoids. We demonstrate that these effects can also occur in aphid‐free plants but only when they are connected to aphid‐infested plants via a common mycorrhizal mycelial network. This underground messaging system allows neighbouring plants to invoke herbivore defences before attack. Our findings demonstrate that common mycorrhizal mycelial networks can determine the outcome of multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbivores and their natural enemies.     

Arbuscular Mycorrhizas: Drivers or Passengers of Alien Plant Invasion

Observational and manipulative studies have revealed that alien plant invasions are an outcome of interplay between a myriad of biotic and abiotic factors operating at various spatio-temporal stages and scales. Despite the salient role of ubiquitous arbuscular mycorrhizal (AM) fungi in plant interactions, studies exploring the role of such symbionts in invasiveness of alien species and invasibility of communities are limited, in part because of difficult-culturablilty of AM fungi on artificial media and apparent complexities in manipulations of AM-plant interactions in field and laboratory experiments. Moreover, analysis of the AM-plant invasion studies conducted so far have yielded contradictory results with some indicating facilitation of invasion by AM fungi and others its inhibition. Other studies have indicated that arbuscular mycorrhizal symbiosis has no effect on invasiveness of alien plants. While arbuscular mycorrhizas may facilitate invasiveness of some alien plants, such plants may also potentially impact mycorrhizal community structure and functions in the invaded habitats in different ways. The present review addresses these paradoxically conflicting observations in the context of mutualism-commensalism-parasitism gradient that characterizes the relationship between AM fungi and their alien vs. native hosts and also discusses the influence of alien invasive plants on mycorrhizal community structure of invaded ecosystems. Through critical analysis of costs and benefits for invasive plants that associate with AM fungi in their introduced range, invasion-induced shifts in AM mutualism are evaluated in the context of their impact on native biodiversity. Underlining limitations of methodologies and experimental designs usually employed to understand AM-mediated plant invasiveness, we proposes herein some alternative frameworks and experimental approaches to overcome these limitations.     

Root endophyte symbiosis in vitro between the ectomycorrhizal basidiomycete Tricholoma matsutake and the arbuscular mycorrhizal plant Prunus speciosa

We previously reported that Tricholoma matsutake and Tricholoma fulvocastaneum, ectomycorrhizal basidiomycetes that associate with Pinaceae and Fagaceae, respectively, in the Northern Hemisphere, could interact in vitro as a root endophyte of somatic plants of Cedrela odorata (Meliaceae), which naturally harbors arbuscular mycorrhizal fungi in South America, to form a characteristic rhizospheric colony or “shiro”. We questioned whether this phenomenon could have occurred because of plant–microbe interactions between geographically separated species that never encounter one another in nature. In the present study, we document that these fungi formed root endophyte interactions and shiro within 140 days of inoculation with somatic plants of Prunus speciosa (=Cerasus speciosa, Rosaceae), a wild cherry tree that naturally harbors arbuscular mycorrhizal fungi in Japan. Compared with C. odorata, infected P. speciosa plants had less mycelial sheath surrounding the exodermis, and the older the roots, especially main roots, the more hyphae penetrated. In addition, a large number of juvenile roots were not associated with hyphae. We concluded that such root endophyte interactions were not events isolated to the interactions between exotic plants and microbes but could occur generally in vitro. Our pure culture system with a somatic plant allowed these fungi to express symbiosis-related phenotypes that varied with the plant host; these traits are innately programmed but suppressed in nature and could be useful in genetic analyses of plant–fungal symbiosis.     

Specificity of assemblage,not fungal partner species,explains mycorrhizal partnerships of mycoheterotrophic Burmannia plants

Mycoheterotrophic plants (MHPs) growing on arbuscular mycorrhizal fungi (AMF) usually maintain specialized mycorrhizal associations. The level of specificity varies between MHPs, although it remains largely unknown whether interactions with mycorrhizal fungi differ by plant lineage, species, and/or by population. Here, we investigate the mycorrhizal interactions among Burmannia species (Burmanniaceae) with different trophic modes using high-throughput DNA sequencing. We characterized the inter- and intraspecific dynamics of the fungal communities by assessing the composition and diversity of fungi among sites. We found that fully mycoheterotrophic species are more specialized in their fungal associations than chlorophyllous species, and that this specialization possibly results from the gradual loss of some fungal groups. In particular, although many fungal species were shared by different Burmannia species, fully MHP species typically host species-specific fungal assemblages, suggesting that they have a preference for the selected fungi. Although no apparent cophylogenetic relationship was detected between fungi and plants, we observe that evolutionarily closely related plants tend to have a greater proportion of shared or closely related fungal partners. Our findings suggest a host preference and specialization toward fungal assemblages in Burmannia, improving understanding of interactions between MHPs and fungi.Subject terms: Fungi, Plant sciences, Evolution     

Plant-plant interactions vary with different mycorrhizal fungus species

Because different species of mycorrhizal fungi have different effects on the growth of particular plant species, variation in mycorrhizal fungus species composition could cause changes in the strength of plant-plant interactions. Results are presented from a growth chamber experiment that compared the strength of interactions among seedlings of ponderosa pine (Pinus ponderosa) when the pines were colonized by two different groups of ectomycorrhizal fungi in the genus Rhizopogon. Plant density effects differed between the two groups of mycorrhizal fungi: plant growth was low regardless of density when plants were colonized with pine-specific Rhizopogon species, while plant growth declined with plant density when plants were colonized by Rhizopogon species having a broader host range. This result parallels results from previous studies showing that plant interactions are more antagonistic with mycorrhizal fungi than without, implying that plant responsiveness to beneficial mycorrhizal fungi declines with increasing plant density. If such effects are prevalent in plant communities, then variation in mycorrhizal fungus community composition is predicted to have a density-dependent effect on plants.     

Arbuscular mycorrhizal fungal communities change among three stages of primary sand dune succession but do not alter plant growth

Plant interactions with soil biota could have a significant impact on plant successional trajectory by benefiting plants in a particular successional stage over others. The influence of soil mutualists such as mycorrhizal fungi is thought to be an important feedback component, yet they have shown benefits to both early and late successional plants that could either retard or accelerate succession. Here we first determine if arbuscular mycorrhizal (AM) fungi differ among three stages of primary sand dune succession and then if they alter growth of plants from particular successional stages. We isolated AM fungal inoculum from early, intermediate or late stages of a primary dune succession and compared them using cloning and sequencing. We then grew eight plant species that dominate within each of these successional stages with each AM fungal inoculum. We measured fungal growth to assess potential AM functional differences and plant growth to determine if AM fungi positively or negatively affect plants. AM fungi isolated from early succession were more phylogenetically diverse relative to intermediate and late succession while late successional fungi consistently produced more soil hyphae and arbuscules. Despite these differences, inocula from different successional stages had similar effects on the growth of all plant species. Host plant biomass was not affected by mycorrhizal inoculation relative to un‐inoculated controls. Although mycorrhizal communities differ among primary dune successional stages and formed different fungal structures, these differences did not directly affect the growth of plants from different dune successional stages in our experiment and therefore may be less likely to directly contribute to plant succession in sand dunes.     

Effects of arbuscular mycorrhizal fungi and a non-pathogenic<Emphasis Type="Italic"> Fusarium oxysporum</Emphasis> on<Emphasis Type="Italic"> Meloidogyne incognita</Emphasis> infestation of tomato

Arbuscular mycorrhizal (AM) fungi and non-pathogenic strains of soil-borne pathogens have been shown to control plant parasitic nematodes. As AM fungi and non-pathogenic fungi improve plant health by different mechanisms, combination of two such partners with complementary mechanisms might increase overall control efficacy and, therefore, provide an environmentally safe alternative to nematicide application. Experiments were conducted to study possible interactions between the AM fungus Glomus coronatum and the non-pathogenic Fusarium oxysporum strain Fo162 in the control of Meloidogyne incognita on tomato. Pre-inoculation of tomato plants with G. coronatum or Fo162 stimulated plant growth and reduced M. incognita infestation. Combined application of the AM fungus and Fo162 enhanced mycorrhization of tomato roots but did not increase overall nematode control or plant growth. A higher number of nematodes per gall was found for mycorrhizal than non-mycorrhizal plants. In synergisms between biocontrol agents, differences in their antagonistic mechanisms seem to be less important than their effects on different growth stages of the pathogen.     

The ecology and evolution of host-plant resistance to insects

Genetic techniques have yielded new insights into plant-herbivore coevolution. Quantitative genetic tests of herbivory theory reveal that in some cases insect herbivores impose selection on resistance traits. Also, some resistance traits are costly while others appear not to be, and genetic models can explain these results. Genetic variation in plant resistance influences insect community structure by modifying interactions of herbivores with competitors and natural enemies. Therefore, models of multispecies coevolution are more realistic than pairwise coevolutionary models. Ecological genetics will facilitate further theoretical and empirical exploration of multispecies coevolution of plants and herbivores.     

菌根真菌多样性与植物多样性的相互作用研究进展

菌根共生双方多样性影响着生态系统的过程与功能。菌根真菌-寄主植物之间的共生组合存在偏好性或特异性,这导致菌根真菌对寄主植物的效益差异和寄主植物对菌根真菌的利益差别：两者在互利共生过程中不仅相互选择,还存在相互促进与制约的关系(如互补与选择效应、竞争),从而在一定程度上决定生态系统的演化与发展。本文概述了植物多样性与菌根真菌多样性的相互影响,探讨了两者互作可能存在的调控因素与机制,对存在的问题和争议进行了总结,并提出了进一步研究的方向。深入阐明植物多样性与菌根真菌多样性之间的互作关系,将丰富生物共生学理论,增强菌根应用潜力及生物多样性的维持。     

Effects of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions

Complex relationships occur among plants, mycorrhizal fungi, and herbivores. By altering plant nutrient status, mycorrhizas may alter herbivory or plant tolerance to herbivory via compensatory regrowth. We examined these interactions by assessing grasshopper preference and plant growth and fungal colonization responses to herbivory under mycorrhizal and non‐mycorrhizal conditions within tallgrass prairie microcosms. Mycorrhizal symbiosis increased plant regrowth following defoliation, and some strongly mycotrophic plant species showed overcompensation in response to herbivory when they were mycorrhizal. Although grasshoppers spent more time on mycorrhizal plants, herbivory intensity did not differ between mycorrhizal and non‐mycorrhizal plants. Aboveground herbivory by grasshoppers significantly increased mycorrhizal fungal colonization of plant roots. Thus mycorrhizas may greatly benefit plants subjected to herbivory by stimulating compensatory growth, and herbivores, in turn, may increase the development of the symbiosis. Our results also indicate strong interspecific differences among tallgrass prairie plant species in their responses to the interaction of aboveground herbivores and mycorrhizal symbionts.     

Potential impacts of multiple partners on mycorrhizal community dynamics

The significance of arbuscular mycorrhizal (AM) fungi in terrestrial ecosystems is widely acknowledged, but the causes and consequences of diversity in these fungi are not well understood. A recent frequency-dependent model suggests that dynamics within mycorrhizal mutualisms could promote the coexistence of at least two competing plant species and two competing fungal species within a community. Models are developed here in which simultaneous association with multiple partners may result in elevated or depressed fitness relative to association with either partner alone. This increases the range of conditions under which negative feedback occurs and coexistence of all four species is possible. Differences between plants in the relative proportions of fungi at which maximum fitness occurs may facilitate coexistence, as may differences between fungi in their abilities to establish interplant connections. These models suggest additional mechanisms by which mutualistic interactions could promote local diversity of plants and AM fungi.     

Diversity and classification of mycorrhizal associations

Most mycorrhizas are 'balanced' mutualistic associations in which the fungus and plant exchange commodities required for their growth and survival. Myco-heterotrophic plants have 'exploitative' mycorrhizas where transfer processes apparently benefit only plants. Exploitative associations are symbiotic (in the broad sense), but are not mutualistic. A new definition of mycorrhizas that encompasses all types of these associations while excluding other plant-fungus interactions is provided. This definition recognises the importance of nutrient transfer at an interface resulting from synchronised plant-fungus development. The diversity of interactions between mycorrhizal fungi and plants is considered. Mycorrhizal fungi also function as endophytes, necrotrophs and antagonists of host or non-host plants, with roles that vary during the lifespan of their associations. It is recommended that mycorrhizal associations are defined and classified primarily by anatomical criteria regulated by the host plant. A revised classification scheme for types and categories of mycorrhizal associations defined by these criteria is proposed. The main categories of vesicular-arbuscular mycorrhizal associations (VAM) are 'linear' or 'coiling', and of ectomycorrhizal associations (ECM) are 'epidermal' or 'cortical'. Subcategories of coiling VAM and epidermal ECM occur in certain host plants. Fungus-controlled features result in 'morphotypes' within categories of VAM and ECM. Arbutoid and monotropoid associations should be considered subcategories of epidermal ECM and ectendomycorrhizas should be relegated to an ECM morphotype. Both arbuscules and vesicles define mycorrhizas formed by glomeromycotan fungi. A new classification scheme for categories, subcategories and morphotypes of mycorrhizal associations is provided.     

Fungal‐host diversity among mycoheterotrophic plants increases proportionally to their fungal‐host overlap

The vast majority of plants obtain an important proportion of vital resources from soil through mycorrhizal fungi. Generally, this happens in exchange of photosynthetically fixed carbon, but occasionally the interaction is mycoheterotrophic, and plants obtain carbon from mycorrhizal fungi. This process results in an antagonistic interaction between mycoheterotrophic plants and their fungal hosts. Importantly, the fungal‐host diversity available for plants is restricted as mycoheterotrophic interactions often involve narrow lineages of fungal hosts. Unfortunately, little is known whether fungal‐host diversity may be additionally modulated by plant–plant interactions through shared hosts. Yet, this may have important implications for plant competition and coexistence. Here, we use DNA sequencing data to investigate the interaction patterns between mycoheterotrophic plants and arbuscular mycorrhizal fungi. We find no phylogenetic signal on the number of fungal hosts nor on the fungal hosts shared among mycoheterotrophic plants. However, we observe a potential trend toward increased phylogenetic diversity of fungal hosts among mycoheterotrophic plants with increasing overlap in their fungal hosts. While these patterns remain for groups of plants regardless of location, we do find higher levels of overlap and diversity among plants from the same location. These findings suggest that species coexistence cannot be fully understood without attention to the two sides of ecological interactions.     

Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes

Most organisms engage in beneficial interactions with other species; however, little is known regarding how individuals balance the competing demands of multiple mutualisms. Here we examine three-way interactions among a widespread grass, Schedonorus phoenix , a protective fungal endophyte aboveground, Neotyphodium coenophialum , and nutritional symbionts (arbuscular mycorrhizal fungi) belowground. In a greenhouse experiment, we manipulated the presence/absence of both fungi and applied a fertilizer treatment to individual plants. Endophyte presence in host plants strongly reduced mycorrhizal colonization of roots. Additionally, for plants with the endophyte, the density of endophyte hyphae was negatively correlated with mycorrhizal colonization, suggesting a novel role for endophyte abundance in the interaction between the symbionts. Endophyte presence increased plant biomass, and there was a positive correlation between endophyte hyphal density and plant biomass. The effects of mutualists were asymmetric: mycorrhizal fungi treatments had no significant impact on the endophyte and negligible effects on plant biomass. Fertilization affected all three species – increasing plant biomass and endophyte density, but diminishing mycorrhizal colonization. Mechanisms driving negative effects of endophytes on mycorrhizae may include inhibition via endophyte alkaloids, altered nutritional requirements of the host plant, and/or temporal and spatial priority effects in the interactions among plants and multiple symbionts.     

Evidence for the evolution of native plant response to mycorrhizal fungi in post‐agricultural grasslands

Plant–microbe interactions play an important role in structuring plant communities. Arbuscular mycorrhizal fungi (AMF) are particularly important. Nonetheless, increasing anthropogenic disturbance will lead to novel plant–AMF interactions, altering longstanding co‐evolutionary trajectories between plants and their associated AMF. Although emerging work shows that plant–AMF response can evolve over relatively short time scales due to anthropogenic change, little work has evaluated how plant AMF response specificity may evolve due to novel plant–mycorrhizal interactions. Here, we examine changes in plant–AMF interactions in novel grassland systems by comparing the mycorrhizal response of plant populations from unplowed native prairies with populations from post‐agricultural grasslands to inoculation with both native prairie AMF and non‐native novel AMF. Across four plant species, we find support for evolution of differential responses to mycorrhizal inocula types, that is, mycorrhizal response specificity, consistent with expectations of local adaptation, with plants from native populations responding most to native AMF and plants from post‐agricultural populations responding most to non‐native AMF. We also find evidence of evolution of mycorrhizal response in two of the four plant species, as overall responsiveness to AMF changed from native to post‐agricultural populations. Finally, across all four plant species, roots from native prairie populations had lower levels of mycorrhizal colonization than those of post‐agricultural populations. Our results report on one of the first multispecies assessment of local adaptation to AMF. The consistency of the responses in our experiment among four species provides evidence that anthropogenic disturbance may have unintended impacts on native plant species'' association with AMF, causing evolutionary change in the benefit native plant species gain from native symbioses.     

Interrelated effects of mycorrhiza and free‐living nitrogen fixers cascade up to aboveground herbivores

Aboveground plant performance is strongly influenced by belowground microorganisms, some of which are pathogenic and have negative effects, while others, such as nitrogen‐fixing bacteria and arbuscular mycorrhizal fungi, usually have positive effects. Recent research revealed that belowground interactions between plants and functionally distinct groups of microorganisms cascade up to aboveground plant associates such as herbivores and their natural enemies. However, while functionally distinct belowground microorganisms commonly co‐occur in the rhizosphere, their combined effects, and relative contributions, respectively, on performance of aboveground plant‐associated organisms are virtually unexplored. Here, we scrutinized and disentangled the effects of free‐living nitrogen‐fixing (diazotrophic) bacteria Azotobacter chroococcum (DB) and arbuscular mycorrhizal fungi Glomus mosseae (AMF) on host plant choice and reproduction of the herbivorous two‐spotted spider mite Tetranychus urticae on common bean plants Phaseolus vulgaris. Additionally, we assessed plant growth, and AMF and DB occurrence and density as affected by each other. Both AMF alone and DB alone increased spider mite reproduction to similar levels, as compared to the control, and exerted additive effects under co‐occurrence. These effects were similarly apparent in host plant choice, that is, the mites preferred leaves from plants with both AMF and DB to plants with AMF or DB to plants grown without AMF and DB. DB, which also act as AMF helper bacteria, enhanced root colonization by AMF, whereas AMF did not affect DB abundance. AMF but not DB increased growth of reproductive plant tissue and seed production, respectively. Both AMF and DB increased the biomass of vegetative aboveground plant tissue. Our study breaks new ground in multitrophic belowground–aboveground research by providing first insights into the fitness implications of plant‐mediated interactions between interrelated belowground fungi–bacteria and aboveground herbivores.     

Mycorrhizal symbiosis increases the benefits of plant facilitative interactions

The diversity of pathways through which mycorrhizal fungi alter plant coexistence hinders the understanding of their effects on plant‐plant interactions. The outcome of plant facilitative interactions can be indirectly affected by mycorrhizal symbiosis, ultimately shaping biodiversity patterns. We tested whether mycorrhizal symbiosis enhances plant facilitative interactions and whether its effect is consistent across different methodological approaches and biological scenarios. We conducted a meta‐analysis of 215 cases (involving 21 nurse and 29 facilitated species), in which the performance of a facilitated plant species is measured in the presence or absence of mycorrhizal fungi. We show that mycorrhizal fungi significantly enhance plant facilitative interactions mainly through an increment in plant biomass (aboveground) and nutrient content, although their effects differ across biological contexts. In semiarid environments mycorrhizal symbiosis enhances plant facilitation, while its effect is non‐significant in temperate ecosystems. In addition, arbuscular but not ecto‐mycorrhizal (EMF) fungi significantly enhance plant facilitation, particularly increasing the P content of the plants more than EMF. Some knowledge gaps regarding the importance of this phenomenon have been detected in this meta‐analysis. The effect of mycorrhizal symbiosis on plant facilitation has rarely been assessed in other ecosystems different from semiarid and temperate forests, and rarely considering other fungal benefits provided to plants besides nutrients. Finally, we are still far from understanding the effects of the whole fungal community on plant‐plant interactions, and on plant species coexistence.     

Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas

1.  A major benefit of the mycorrhizal symbiosis is that it can protect plants from below-ground enemies, such as pathogens. Previous studies have indicated that plant identity (particularly plants that differ in root system architecture) or fungal identity (fungi from different families within the Glomeromycota) can determine the degree of protection from infection by pathogens. Here, we test the combined effects of plant and fungal identity to assess if there is a strong interaction between these two factors.
2.  We paired one of two plants ( Setaria glauca , a plant with a finely branched root system and Allium cepa , which has a simple root system) with one of six different fungal species from two families within the Glomeromycota. We assessed the degree to which plant identity, fungal identity and their interaction determined infection by Fusarium oxysporum , a common plant pathogen.
3.  Our results show that the interaction between plant and fungal identity can be an important determinant of root infection by the pathogen. Infection by Fusarium was less severe in Allium (simple root system) or when Setaria (complex root system) was associated with a fungus from the family Glomeraceae. We also detected significant plant growth responses to the treatments; the fine-rooted Setaria benefited more from associating with a member of the family Glomeraceae, while Allium benefited more from associating with a member of the family Gigasporaceae.
4.   Synthesis . This study supports previous claims that plants with complex root systems are more susceptible to infection by pathogens, and that the arbuscular mycorrhizal symbiosis can reduce infection in such plants – provided that the plant is colonized by a mycorrhizal fungus that can offer protection, such as the isolates of Glomus used here.     

How do belowground organisms influence plant-pollinator interactions?

Aims The majority of angiosperms are pollinated by animals, and this interaction is of enormous importance in both agricultural and natural systems. Pollinator behavior is influenced by plants' floral traits, and these traits may be modified by interactions with other community members. In recent years, knowledge of ecological linkages between above- and belowground organisms has grown tremendously. Soil communities are extremely diverse, and when their interactions with plants influence floral characteristics, they have the potential to alter pollinator attraction and visitation, but plant–pollinator interactions have been neglected in studies of the direct and indirect effects of soil organism–root interactions. Here, we review these belowground interactions, focusing on the effects of nitrogen-fixing bacteria, arbuscular mycorrhizal fungi and root-feeding herbivores, and their effects on floral traits and pollinators. Further, we identify gaps in our knowledge of these indirect effects and recommend promising directions and topics that should be addressed by future research.Important findings Belowground organisms can influence a wide variety of floral traits that are important mediators of pollinator attraction, including the number and size of flowers and nectar and pollen production. Other traits that are known to influence pollinators in some plant species, such as floral volatiles, color and nectar composition, have rarely or never been examined in the context of belowground plant interactions. Despite clear effects on flowers, relatively few studies have measured pollinator responses to belowground interactions. When these indirect effects have been studied, both arbuscular mycorrhizal fungi and root herbivores were found to shift pollinator visitation patterns. Depending on the interaction, these changes may either increase or decrease pollinator attraction. Finally, we discuss future directions for ecological studies that will more fully integrate belowground ecology with pollination biology. We advocate a multilevel approach to these questions to not only document indirect effect pathways between soil interactions and pollination but also identify the mechanisms driving changes in pollinator impacts and the resultant effects on plant fitness. A more thorough understanding of these indirect interactions will advance ecological theory and may inform management strategies in agriculture and conservation biology.