Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence

Numerical models have suggested that the dynamics within mutualisms are not important for the maintenance of diversity. In this study it is demonstrated that the dynamics within mutualism can contribute to the maintenance of diversity within its participants, using a general model of frequency dependence between two mutualistically interacting guilds. Specifically, it is demonstrated that while mutualisms may exhibit positive feedback in density, there may be a negative feedback within a mutualism as a result of the change in composition within the interacting guild. Such a negative feedback results from an asymmetry in the delivery of benefit between participants of the mutualism that generates a negative interguild frequency dependence. This dynamic contributes to the maintenance of diversity within the interacting guilds. Conditions are identified for the maintenance of diversity and the maximization of benefit from mutualism within the context of the model. The utility of these conditions for testing hypotheses using data from the mutualistic interaction between plants and mycorrhizal fungi is then demonstrated.     

Options of partners improve carbon for phosphorus trade in the arbuscular mycorrhizal mutualism

The mutualism between plants and arbuscular mycorrhizal fungi (AMF) is widespread and has persisted for over 400 million years. Although this mutualism depends on fair resource exchange between plants and fungi, inequality exists among partners despite mechanisms that regulate trade. Here, we use ³³P and ¹⁴C isotopes and a split‐root system to test for preferential allocation and reciprocal rewards in the plant–AMF symbiosis by presenting a plant with two AMF that differ in cooperativeness. We found that plants received more ³³P from less cooperative AMF in the presence of another AMF species. This increase in ³³P resulted in a reduced ¹⁴C cost per unit of ³³P from less cooperative AMF when alternative options were available. Our results indicate that AMF diversity promotes cooperation between plants and AMF, which may be an important mechanism maintaining the evolutionary persistence of and diversity within the plant–AMF mutualism.     

Specificity in host-fungus associations: Do mutualists differ from antagonists?

Summary Physically intimate interactions between organisms are assumed to be highly specific, yet intimate mutualisms exhibiting little specificity are common and important in many communities. We compare host records for ectomycorrhizal fungi (mutualists) to those for biotrophic shoot fungi and necrotrophic root fungi (both antagonists) in order to test two alternative predictions: (1) intimate physical associations (biotrophy) are more specific than less intimate ones (necrotrophy); (2) antagonisms are more specific than mutualisms. Specificity of fungi for hosts supports prediction (1): ectomycorrhizal fungi and shoot biotrophs are more host specific than root necrotrophs. Fungal symbiont ranges of hosts supports prediction (2): woody hosts are associated with a greater number of mutualistic fungi than antagonistic fungi. The numbers of fungi in the three groups infecting hosts are all significantly positively correlated. This result suggests that some hosts are resistant to fungal invasion and others are quite susceptible. Thus, plants may not be able to erect selective barriers to only antagonistic fungi. The marked asymmetry of specificity from the perspectives of hosts vs fungi suggests that evolutionary and ecological processes act differently on partners in symbioses.     

Ecological specialization and trade affect the outcome of negotiations in mutualism

By definition, mutualisms involve the exchange of goods or services between partners. It has been shown that mutualism can grade into parasitism, but even when exchange is mutually beneficial, a conflict of interest remains because each partner benefits from reaping more benefits at a lower cost. Metaphorically, the partners negotiate the conditions of trade, the outcome of which will determine the net benefit to each partner. Each partner can adjust its allocation to self-provisioning while negotiating the ratio at which benefits are exchanged. To understand how these two features of trade affect mutualisms, we used the example of the plant-arbuscular mycorrhizal mutualism and modeled uptake and trade of two resources, phosphorus and carbon. In most contexts, the fungus specialized on phosphorus uptake while the plant took up both phosphorus and carbon. However, when phosphorus was abundant and light was scarce, the plant specialized, taking up only carbon and relying on trade for phosphorus. Resource availability was the most important factor determining specialization and the outcome of negotiation and trade, but other aspects of the context were also important. These results suggest experiments to link these two key features of trade with environmental conditions to determine the outcome of mutualism.     

Nutrient loading alters the performance of key nutrient exchange mutualisms

Nutrient exchange mutualisms between phototrophs and heterotrophs, such as plants and mycorrhizal fungi or symbiotic algae and corals, underpin the functioning of many ecosystems. These relationships structure communities, promote biodiversity and help maintain food security. Nutrient loading may destabilise these mutualisms by altering the costs and benefits each partner incurs from interacting. Using meta‐analyses, we show a near ubiquitous decoupling in mutualism performance across terrestrial and marine environments in which phototrophs benefit from enrichment at the expense of their heterotrophic partners. Importantly, heterotroph identity, their dependence on phototroph‐derived C and the type of nutrient enrichment (e.g. nitrogen vs. phosphorus) mediated the responses of different mutualisms to enrichment. Nutrient‐driven changes in mutualism performance may alter community organisation and ecosystem processes and increase costs of food production. Consequently, the decoupling of nutrient exchange mutualisms via alterations of the world's nitrogen and phosphorus cycles may represent an emerging threat of global change.     

As you reap, so shall you sow: coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi

At present there is no consensus theory explaining the evolutionary stability of mutualistic interactions. However, the question is whether there are general 'rules', or whether each particular mutualism needs a unique explanation. Here, I address the ultimate evolutionary stability of the 'agricultural' mutualism between fungus-growing termites and Termitomyces fungi, and provide a proximate mechanism for how stability is achieved. The key to the proposed mechanism is the within-nest propagation mode of fungal symbionts by termites. The termites suppress horizontal fungal transmission by consuming modified unripe mushrooms (nodules) for food. However, these nodules provide asexual gut-resistant spores that form the inoculum of new substrate. This within-nest propagation has two important consequences: (i) the mutualistic fungi undergo severe, recurrent bottlenecks, so that the fungus is likely to be in monoculture and (ii) the termites 'artificially' select for high nodule production, because their fungal food source also provides the inoculum for the next harvest. I also provide a brief comparison of the termite-fungus mutualism with the analogous agricultural mutualism between attine ants and fungi. This comparison shows that--although common factors for the ultimate evolutionary stability of mutualisms can be identified--the proximate mechanisms can be fundamentally different between different mutualisms.     

Hiding in a crowd—does diversity facilitate persistence of a low-quality fungal partner in the mycorrhizal symbiosis?

Given that arbuscular mycorrhizal (AM) fungi are not consistently beneficial to their host plants, it is difficult to explain the evolutionary persistence of this relationship. We tested the hypothesis that increasing either fungal or host biodiversity allows an AM fungus to persist on a host where it shows little benefit. We found that growing such a fungus (an isolate of Glomus custos associating with Plantago laceolata) in combination with certain fungi improved its success as measured by mtLSU DNA abundance. Increasing plant species richness facilitated the spread of this fungus as measured by spore density and fungal colonization; the role of host species richness was not as clear when looking at measures of root abundance. These results indicate that diversity in the AM symbiosis, both plant and fungal, can promote the persistence of low-quality fungi. By existing within a complex mycelial network fungal strains that show little growth benefit to their hosts have a better chance of persisting on that same host. This has the potential to promote selection for heterogeneous AM fungal communities on a small spatial scale.     

Arbuscular Mycorrhizal Fungal Networks Vary throughout the Growing Season and between Successional Stages

To date, few analyses of mutualistic networks have investigated successional or seasonal dynamics. Combining interaction data from multiple time points likely creates an inaccurate picture of the structure of networks (because these networks are aggregated across time), which may negatively influence their application in ecosystem assessments and conservation. Using a replicated bipartite mutualistic network of arbuscular mycorrhizal (AM) fungal-plant associations, detected using large sample numbers of plants and AM fungi identified through molecular techniques, we test whether the properties of the network are temporally dynamic either between different successional stages or within the growing season. These questions have never been directly tested in the AM fungal-plant mutualism or the vast majority of other mutualisms. We demonstrate the following results: First, our examination of two different successional stages (young and old forest) demonstrated that succession increases the proportion of specialists within the community and decreases the number of interactions. Second, AM fungal-plant mutualism structure changed throughout the growing season as the number of links between partners increased. Third, we observed shifts in associations between AM fungal and plant species throughout the growing season, potentially reflecting changes in biotic and abiotic conditions. Thus, this analysis opens up two entirely new areas of research: 1) identifying what influences changes in plant-AM fungal associations in these networks, and 2) what aspects of temporal variation and succession are of general importance in structuring bipartite networks and plant-AM fungal communities.     

Host specificity in ectomycorrhizal communities: what do the exceptions tell us?

Classic ectomycorrhizal symbioses are mutualisms that involvethe exchange of fixed carbon for mineral nutrients between plantroots and fungi. They are unique in the way they contain featuresof both intimate and diffuse symbioses. The degree of host specificityvaries, particularly among the fungi. Here we examine two exceptionalcases of specificity to see what they tell us about the advantagesof specificity, how it is initiated, and the potential rolethat it plays in complex ecosystems. The first case involvesnon-photosynthetic epiparasitic plants, which contrary to virtuallyall other plants, exhibit high levels of specificity towardtheir fungal hosts. The second case involves suilloid fungi;this is the largest monophyletic group of ectomycorrhizal fungithat is essentially restricted to associations with a singleplant family. In both cases, new symbioses are initiated bydormant propagules that are stimulated to germinate by chemicalcues from the host. This reduces the cost of wasting propaguleson non-hosts. The advantages of specificity remain unclear inboth cases, but we argue that increased benefit to the specialistmay result from specialized physiological adaptations. We reexaminethe idea that specialist fungi may help their hosts competein complex ecosystems by reducing facultative epiparasitismby other plants, and suggest an alternative hypothesis for theobserved pattern.     

A facultative mutualism between aphids and an invasive ant increases plant reproduction

1. The consequences to plants of ant–aphid mutualisms, particularly those involving invasive ants, are poorly studied. Ant–aphid mutualisms may increase or decrease plant fitness depending on the relative cost of herbivory by ant‐tended aphids versus the relative benefit of increased ant suppression of other (non‐aphid) herbivores. 2. We conducted field and greenhouse experiments in which we manipulated the presence and absence of cotton aphids (Aphis gossypii) on cotton plants to test the hypothesis that a mutualism between cotton aphids and an invasive ant, the red imported fire ant (Solenopsis invicta), benefits cotton plants by increasing fire ant suppression of caterpillars. We also manipulated caterpillar abundance to test whether the benefit of the mutualism varied with caterpillar density. 3. We found that more fire ants foraged on plants with cotton aphids than on plants without cotton aphids, which resulted in a significant reduction in caterpillar survival and caterpillar herbivory of leaves, flower buds, and bolls on plants with aphids. Consequently, cotton aphids indirectly increased cotton reproduction: plants with cotton aphids produced 16% more bolls, 25% more seeds, and 10% greater seedcotton mass than plants without aphids. The indirect benefit of cotton aphids, however, varied with caterpillar density: the number of bolls per plant at harvest was 32% greater on plants with aphids than on plants without aphids at high caterpillar density, versus just 3% greater at low caterpillar density. 4. Our results highlight the potential benefit to plants that host ant–hemipteran mutualisms and provide the first experimental evidence that the consequences to plants of an ant–aphid mutualism vary at different densities of non‐aphid herbivores.     

Phylogenetic trait conservation in the partner choice of a group of ectomycorrhizal trees

Ecological interactions are frequently conserved across evolutionary time. In the case of mutualisms, these conserved interactions may play a large role in structuring mutualist communities. We hypothesized that phylogenetic trait conservation could play a key role in determining patterns of association in the ectomycorrhizal symbiosis, a globally important trophic mutualism. We used the association between members of the pantropical plant tribe Pisonieae and its fungal mutualist partners as a model system to test the prediction that Pisonieae‐associating ectomycorrhizal fungi will be more closely related than expected by chance, reflecting a conserved trait. We tested this prediction using previously published and newly generated sequences in a Bayesian framework incorporating phylogenetic uncertainty. We report that phylogenetic trait conservation does exist in this association. We generated a five‐marker phylogeny of members of the Pisonieae and used this phylogeny in a Bayesian relaxed molecular clock analysis. We established that the most recent common ancestors of Pisonieae species and Pisonieae‐associating fungi sharing phylogenetic conservation of their patterns of ectomycorrhizal association occurred no more recently than 14.2 Ma. We therefore suggest that phylogenetic trait conservation in the Pisonieae ectomycorrhizal mutualism association represents an inherited syndrome which has existed for at least 14 Myr.     

Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae)

About half a dozen obligate pollination mutualisms between plants and their seed-consuming pollinators are currently recognized, including fig-fig wasp, yucca-yucca moth, and the recently discovered Glochidion tree-Epicephala moth mutualisms. A common principle among these interactions is that the pollinators consume only a limited amount of the seed crop within a developing fruit (or fig in the case of fig-fig wasp mutualism), thereby ensuring a net benefit to plant reproduction. A novel obligate, seed-parasitic pollination mutualism between two species of New Caledonian Phyllanthus (Euphorbiaceae), a close relative of Glochidion, and Epicephala moths (Gracillariidae) is an exception to this principle. The highly specialized flowers of Phyllanthus are actively and exclusively pollinated by species-specific Epicephala moths, whose larvae consume all six ovules of the developing fruit. Some flowers pollinated by the moths remain untouched, and thus a fraction of the fruits is left intact. Additional evidence for a similar association of Epicephala moths in other Phyllanthus species suggests that this interaction is a coevolved, species-specific pollination mutualism. Implications for the evolutionary stability of the system, as well as differences in mode of interaction with respect to the Glochidion-Epicephala mutualism, are discussed.     

High diversity and low specificity of fungi associated with seedless epiphytic plants

Epiphytes, which grow on other plants for support, make up a large portion of Earth's plant diversity. Like other plants, their surfaces and interiors are colonized by diverse assemblages of fungi that can benefit their hosts by increasing tolerance for abiotic stressors and resistance to disease or harm them as pathogens. Fungal communities associated with epiphytic plants and the processes that structure these communities are poorly known. To address this, we sampled seven epiphytic seedless plant taxa in a Costa Rican rainforest and examined the effects of host identity and microhabitat on external and endophytic fungal communities. We found low host specificity for both external and endophytic fungi and weak differentiation between epiphytic and neighboring epilithic plant hosts. High turnover in fungi within and between hosts and habitats reveals that epiphytic plant-associated fungal communities are highly diverse and suggests that they are structured by stochastic processes.     

Mutualism and adaptive divergence: co-invasion of a heterogeneous grassland by an exotic legume-rhizobium symbiosis

Species interactions play a critical role in biological invasions. For example, exotic plant and microbe mutualists can facilitate each other's spread as they co-invade novel ranges. Environmental context may influence the effect of mutualisms on invasions in heterogeneous environments, however these effects are poorly understood. We examined the mutualism between the legume, Medicago polymorpha, and the rhizobium, Ensifer medicae, which have both invaded California grasslands. Many of these invaded grasslands are composed of a patchwork of harsh serpentine and relatively benign non-serpentine soils. We grew legume genotypes collected from serpentine or non-serpentine soil in both types of soil in combination with rhizobium genotypes from serpentine or non-serpentine soils and in the absence of rhizobia. Legumes invested more strongly in the mutualism in the home soil type and trends in fitness suggested that this ecotypic divergence was adaptive. Serpentine legumes had greater allocation to symbiotic root nodules in serpentine soil than did non-serpentine legumes and non-serpentine legumes had greater allocation to nodules in non-serpentine soil than did serpentine legumes. Therefore, this invasive legume has undergone the rapid evolution of divergence for soil-specific investment in the mutualism. Contrary to theoretical expectations, the mutualism was less beneficial for legumes grown on the stressful serpentine soil than on the non-serpentine soil, possibly due to the inhibitory effects of serpentine on the benefits derived from the interaction. The soil-specific ability to allocate to a robust microbial mutualism may be a critical, and previously overlooked, adaptation for plants adapting to heterogeneous environments during invasion.     

Diversity and Spatial Structure of Belowground Plant–Fungal Symbiosis in a Mixed Subtropical Forest of Ectomycorrhizal and Arbuscular Mycorrhizal Plants

Plant–mycorrhizal fungal interactions are ubiquitous in forest ecosystems. While ectomycorrhizal plants and their fungi generally dominate temperate forests, arbuscular mycorrhizal symbiosis is common in the tropics. In subtropical regions, however, ectomycorrhizal and arbuscular mycorrhizal plants co-occur at comparable abundances in single forests, presumably generating complex community structures of root-associated fungi. To reveal root-associated fungal community structure in a mixed forest of ectomycorrhizal and arbuscular mycorrhizal plants, we conducted a massively-parallel pyrosequencing analysis, targeting fungi in the roots of 36 plant species that co-occur in a subtropical forest. In total, 580 fungal operational taxonomic units were detected, of which 132 and 58 were probably ectomycorrhizal and arbuscular mycorrhizal, respectively. As expected, the composition of fungal symbionts differed between fagaceous (ectomycorrhizal) and non-fagaceous (possibly arbuscular mycorrhizal) plants. However, non-fagaceous plants were associated with not only arbuscular mycorrhizal fungi but also several clades of ectomycorrhizal (e.g., Russula) and root-endophytic ascomycete fungi. Many of the ectomycorrhizal and root-endophytic fungi were detected from both fagaceous and non-fagaceous plants in the community. Interestingly, ectomycorrhizal and arbuscular mycorrhizal fungi were concurrently detected from tiny root fragments of non-fagaceous plants. The plant–fungal associations in the forest were spatially structured, and non-fagaceous plant roots hosted ectomycorrhizal fungi more often in the proximity of ectomycorrhizal plant roots. Overall, this study suggests that belowground plant–fungal symbiosis in subtropical forests is complex in that it includes “non-typical” plant–fungal combinations (e.g., ectomycorrhizal fungi on possibly arbuscular mycorrhizal plants) that do not fall within the conventional classification of mycorrhizal symbioses, and in that associations with multiple functional (or phylogenetic) groups of fungi are ubiquitous among plants. Moreover, ectomycorrhizal fungal symbionts of fagaceous plants may “invade” the roots of neighboring non-fagaceous plants, potentially influencing the interactions between non-fagaceous plants and their arbuscular-mycorrhizal fungal symbionts at a fine spatial scale.     

Trait‐based partner selection drives mycorrhizal network assembly

Plants and their microbial symbionts are often found to interact non‐randomly in nature, but we have yet to understand the mechanisms responsible for such preferential species associations. Theory predicts that host plants should select symbiotic partners bearing traits complementary to their own, as this should favor cooperation and evolutionary stability of mutualisms. Here, we present the first field‐based empirical test for this hypothesis using arbuscular mycorrhizas (AM), the oldest and most widespread plant symbiosis. Preferential associations occurring within a local plant–AM fungal community could not be predicted by the spatial distributions of interacting partners, nor by gradients in soil properties. Rather, plants with similar traits preferentially hosted similar AM fungi and, likewise, phylogenetically related AM fungi (assumed to have similar functional traits) interacted with similar plants. Our results suggest that trait‐based partner selection may have been a strong force in maintaining plant–AM fungal symbioses since the evolution of land plants.     

Carbon allocation and competition maintain variation in plant root mutualisms

Plants engage in multiple root symbioses that offer varying degrees of benefit. We asked how variation in partner quality persists using a resource‐ratio model of population growth. We considered the plant's ability to preferentially allocate carbon to mutualists and competition for plant carbon between mutualist and nonmutualist symbionts. We treated carbon as two nutritionally interchangeable, but temporally separated, resources—carbon allocated indiscriminately for the construction of the symbiosis, and carbon preferentially allocated to the mutualist after symbiosis establishment and assessment. This approach demonstrated that coexistence of mutualists and nonmutualists is possible when fidelity of the plant to the mutualist and the cost of mutualism mediate resource competition. Furthermore, it allowed us to trace symbiont population dynamics given varying degrees of carbon allocation. Specifically, coexistence occurs at intermediate levels of preferential allocation. Our findings are consistent with previous empirical studies as well the application of biological market theory to plantroot symbioses.     

Availability and function of arbuscular mycorrhizal and ectomycorrhizal fungi during revegetation of dewatered reservoirs left after dam removal

Revegetation following dam removal projects may depend on recovery of arbuscular mycorrhizal (AM) and ectomycorrhizal (EM) fungal communities, which perform valuable ecosystem functions. This study assessed the availability and function of AM and EM fungi for plants colonizing dewatered reservoirs following a dam removal project on the Elwha River, Olympic Peninsula, Washington, United States. Availability was assessed via AM fungal spore density in soils and EM root tip colonization of Salix sitchensis (Sitka willow) in an observational field study. The effect of mycorrhizal fungi from 4 sources (reservoir soils, commercial inoculum, and 2 mature plant community soils) on growth and nutrient status of S. sitchensis was quantified in a greenhouse study. AM fungal spores and EM root tips were present in all field samples. In the greenhouse, plants receiving reservoir soil inoculum had only incipient mantle formation, while plants receiving inoculum from mature plant communities had fully formed EM root tips. EM formation corresponded with alleviation of phosphorus stress in plants (lower shoot nitrogen:phosphorus). Thus, revegetating plants have access to AM and EM fungi following dam removal, and EM formation may be especially important for plant P uptake in reservoir soils. However, availability of mycorrhizal fungi declines with distance from established plant communities. Furthermore, EM fungal communities in recently dewatered reservoirs may not be as effective at forming beneficial mycorrhizae as those from mature plant communities. Whole soil inoculum from mature plant communities may be important for the success of revegetating plants and recovery of mycorrhizal fungal communities.     

Compatible host/mycorrhizal fungus combinations for micropropagated sea oats

Micropropagation technology promises to improve the supply of sea oats for restoring Florida's eroded beaches, but concerns about genetic diversity need to be addressed. These dune plants are colonized by a wide array of arbuscular mycorrhizal (AM) fungi, yet little is know of the diversity of these fungal communities. Our goal was to test the level of functional diversity that exists among communities of AM fungi that are present in divergent Florida dunes. Community pot cultures were established from samples collected from ten transects in two Gulf coast and two Atlantic coast locations in Florida, and these were used to conduct two greenhouse studies. The objective of the first study was to evaluate within-location variance in the mycorrhizal function of different AM fungal communities associated with endemic sea oats. The objective of the second study was to evaluate among-location responses of plant and fungal ecotypes using selected combinations obtained from the first experiment. Within locations, the AM fungal community had significant impacts on shoot mass and shoot-P contents, confirming a range of symbiotic effectiveness exists within the beach-dune system. Among locations, there was a tendency for greater root colonization between host clones and fungal communities from the same location, indicating a degree of specificity between host ecotypes and their symbiotic fungi. Relative to plant growth response, one fungal community was superior across plant genotypes from all locations, while one plant genotype tended to have the best response across all fungal communities. These data suggest that while it is possible to select effective AM fungal-host combinations for outplanting, origin of host and AM fungi have little predictive value in screening these combinations.     

Fungal Assemblages Associated with Roots of Halophytic and Non-halophytic Plant Species Vary Differentially Along a Salinity Gradient

Structure of fungal communities is known to be influenced by host plants and environmental conditions. However, in most cases, the dynamics of these variation patterns are poorly understood. In this work, we compared richness, diversity, and composition between assemblages of endophytic and rhizospheric fungi associated to roots of two plants with different lifestyles: the halophyte Inula crithmoides and the non-halophyte I. viscosa (syn. Dittrichia viscosa L.), along a spatially short salinity gradient. Roots and rhizospheric soil from these plants were collected at three points between a salt marsh and a sand dune, and fungi were isolated and characterized by ITS rDNA sequencing. Isolates were classified in a total of 90 operational taxonomic units (OTUs), belonging to 17 fungal orders within Ascomycota and Basidiomycota. Species composition of endophytic and soil communities significantly differed across samples. Endophyte communities of I. crithmoides and I. viscosa were only similar in the intermediate zone between the salt marsh and the dune, and while the latter displayed a single, generalist association of endophytes, I. crithmoides harbored different assemblages along the gradient, adapted to the specific soil conditions. In the lower salt marsh, root assemblages were strongly dominated by a single dark septate sterile fungus, also prevalent in other neighboring salt marshes. Interestingly, although its occurrence was positively correlated to soil salinity, in vitro assays revealed a strong inhibition of its growth by salts. Our results suggest that host lifestyle and soil characteristics have a strong effect on endophytic fungi and that environmental stress may entail tight plant-fungus relationships for adaptation to unfavorable conditions.