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.This work was supported by DEB-1556664 (J.D.B). N.C. was supported by a National Science Foundation Graduate Research Fellowshi

Plant preferential allocation and fungal reward decline with soil phosphorus: implications for mycorrhizal mutualism

Explaining the persistence of mutualism remains a challenge in ecology and evolutionary biology. The evolutionary stability of arbuscular mycorrhiza, a most widespread and ancient mutualistic association, is particularly intriguing because plants lack apparent mechanisms to prevent cheaters from gaining competitive advantages over cooperators. We developed a triple isotopic labeling method (14C, 32P, and 33P) within a split-root design to measure the exchange of carbon (C) and phosphorus (P) between the host plant and two mycorrhizal partners across a soil P gradient. Host plant preferentially allocated more C to the roots associated with the fungus delivering higher P per unit plant C, and the strength of preferential allocation decreased with increasing soil P availability. The host plant received more P per unit of allocated C from the better fungus and this advantageous exchange rate did not depend upon P availability. As a result, the level of preferential allocation was correlated with the differential delivery of P from the two fungi. Our findings suggest that plant preferential allocation to better mutualists can stabilize mutualisms in environments limiting in the traded resource, but as the availability of this resource increases, plant preferential allocation declines. This environmental dependence of preferential allocation generates predictions of declining levels in relative abundance of mutualistic fungi in high-resource environments

Spherical collapse model in agegraphic dark energy cosmologies

Under the commonly used spherical collapse model, we study how dark energy affects the growth of large scale structures of the Universe in the context of agegraphic dark energy models. The dynamics of the spherical collapse of dark matter halos in nonlinear regimes is determined by the properties of the dark energy model. We show that the main parameters of the spherical collapse model are directly affected by the evolution of dark energy in the agegraphic dark energy models. We compute the spherical collapse quantities for different values of agegraphic model parameter $\alpha$ in two different scenarios: first, when dark energy does not exhibit fluctuations on cluster scales, and second, when dark energy inside the overdense region collapses similar to dark matter. Using the Sheth-Tormen and Reed mass functions, we investigate the abundance of dark matter halos in the framework of agegraphic dark energy cosmologies. The model parameter $\alpha$ is a crucial parameter in order to count the abundance of dark matter halos. Specifically, the present analysis suggests that the agegraphic dark energy model with bigger (smaller) value of $\alpha$ predicts less (more) virialized halos with respect to that of $\Lambda$CDM cosmology. We also show that in agegraphic dark energy models, the number of halos strongly depends on clustered or uniformed distributions of dark energy.Comment: 14 pages, 7 figures. Accepted in Physical Review

Mycorrhizal Species Differentially Alter Plant Growth and Response to Herbivory

Plants simultaneously interact with multiple organisms which can both positively and negatively affect their growth. Herbivores can reduce plant growth through loss of plant biomass and photosynthetic area, while plant mutualists, such as mycorrhizal fungi, can increase plant growth through uptake of essential nutrients. This is the first study examining whether species-specific associations with mycorrhizal fungi alter plant tolerance to herbivory. We grew Plantago lanceolata plants with three species of mycorrhizal fungi previously shown to have differential impacts on plant growth and subjected them to herbivory by the specialist lepidopteran herbivore, Junonia coenia. Association with mycorrhizal fungus Glomus white provided the greatest growth benefit but did not alter plant response to herbivory. Alternatively, association with Archaeospora trappei provided less growth promotion but did lead to tolerance to herbivory in the form of an increased growth rate. Finally, an association with the fungus Scutellospora calospora led to neither plant growth promotion nor tolerance to herbivory. In fact, an association with S. calospora appeared to reduce plant tolerance to herbivory. An association with all three species of mycorrhizae resulted in a pattern of growth similar to that of plants grown only with Glomus white, suggesting that growth promotion by multiple mycorrhizal species is driven by the inclusion of a “super fungus,” in this case, Glomus white. This work illustrates that plant response to herbivory depends upon the mycorrhizal fungal mutualist with which a plant is associated

Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion

Belowground interactions between herbaceous native species and nonnative species is a poorly understood but emerging area of interest to invasive-species researchers. Positive feedback dynamics are commonly observed in many invaded systems and have been suspected in California grasslands, where native plants associate strongly with soil mutualists such as arbuscular mycorrhizal fungi. In response to disturbance, invading nonnative plants proliferate, and to the degree these species associate weakly with soil mutualists, we would expect mutualist efficacy to degrade over time. Degraded mutualist efficacy would negatively impact mutualist-dependent native species or their recruitment following a disturbance. We investigated the feedback dynamics of soil conditioned both with native and nonnative herbaceous communities of southern California grasslands to test this degraded mutualist hypothesis. Using a mesocosm approach, we inoculated each community with live soil originating from a remnant native grassland and varied the plant communities (i.e., native or nonnative) along a plant–species-richness gradient. After one year, we then used this conditioned soil for reciprocal feedback tests on a native and nonnative indicator species. We show that a native herbaceous forb (Gnaphalium californicum) grows best in soil conditioned by a diverse mix of other native species that includes G. californicum but is inhibited by soil conditioned by a diverse mix of nonnative species. We also show that an invasive, nonnative herbaceous forb (Carduus pycnocephalus) exhibits strong growth in soil lacking arbuscular mycorrhizal fungi and in soil conditioned by a diverse mix of nonnative species that include C. pycnocephalus, and that it is inhibited by the same soil that best promotes the native, G. californicum. Separate bioassays for mycorrhizal density show a reduction of arbuscular mycorrhizal fungi in the nonnative-conditioned soil relative to the native-conditioned soil, which suggests that nonnative species do not promote the growth of mycorrhizal fungi in the same way that native species do. The growth patterns resulting from the vegetative history of these distinct soil communities provide evidence of a biotic feedback mechanism that may account for the maintenance of persistent communities of nonnative (and often invasive) plants ubiquitous throughout California grasslands

The Coexistence of Hosts with Different Abilities to Discriminate against Cheater Partners: An Evolutionary Game-Theory Approach

Evolutionary theory predicts that mutualisms based on the reciprocal exchange of costly services should be susceptible to exploitation by cheaters. Consistent with theory, both cheating and discrimination against cheaters are ubiquitous features of mutualisms. Several recent studies have confirmed that host species differ in the extent that they are able to discriminate against cheaters, suggesting that cheating may be stabilized by the existence of susceptible hosts (dubbed “givers”). We use an evolutionary game-theoretical approach to demonstrate how discriminating and giver hosts associating with mutualist and cheater partners can coexist. Discriminators drive the proportion of cheaters below a critical threshold, at which point there is no benefit to investing resources into discrimination. This promotes givers, who benefit from mutualists but allow cheater populations to rebound. We then apply this model to the plant-mycorrhizal mutualism and demonstrate it is one mechanism for generating host-specific responses to mycorrhizal fungal species necessary to generate negative plant-soil feedbacks. Our model makes several falsifiable, qualitative predictions for plant-mycorrhizal population dynamics across gradients of soil phosphorus availability and interhost differences in ability to discriminate. Finally, we suggest applications and limitations of the model with regard to coexistence in specific biological systems

Disturbance reduces the differentiation of mycorrhizal fungal communities in grasslands along a precipitation gradient

Given that mycorrhizal fungi play key roles in shaping plant communities, greater attention should be focused on factors that determine the composition of mycorrhizal fungal communities and their sensitivity to anthropogenic disturbance. We investigate changes in arbuscular mycorrhizal (AM) fungal community composition across a precipitation gradient in North American grasslands as well as changes occurring with varying degrees of site disturbance that have resulted in invasive plant establishment. We find strong differentiation of AM fungal communities in undisturbed remnant grasslands across the precipitation gradient, whereas communities in disturbed grasslands were more homogeneous. These changes in community differentiation with disturbance are consistent with more stringent environmental filtering of AM fungal communities in undisturbed sites that may also be promoted by more rigid functional constraints imposed on AM fungi by the native plant communities in these areas. The AM fungal communities in eastern grasslands were particularly sensitive to anthropogenic disturbance, with disturbed sites having low numbers of AM fungal operational taxonomic units (OTUs) commonly found in undisturbed sites, and also the proliferation of AM fungal OTUs in disturbed sites. This proliferation of AM fungi in eastern disturbed sites coincided with increased soil phosphorus availability and is consistent with evidence suggesting the fungi represented by these OTUs would provide reduced benefits to native plants. The differentiation of AM fungal communities along the precipitation gradient in undisturbed grasslands but not in disturbed sites is consistent with AM fungi aiding plant adaptation to climate, and suggests they may be especially important targets for conservation and restoration in order to help maintain or re-establish diverse grassland plant communities.This work was supported by Strategic Environmental Research and Development Program (SERDP) grant RC-2330 to J. D. BeverNational Science Foundation grant DEB-1556664 to J. D. Beve

Joint Evolution of Kin Recognition and Cooperation in Spatially Structured Rhizobium Populations

In the face of costs, cooperative interactions maintained over evolutionary time present a central question in biology. What forces maintain this cooperation? Two potential ways to explain this problem are spatially structured environments (kin selection) and kin-recognition (directed benefits). In a two-locus population genetic model, we investigated the relative roles of spatial structure and kin recognition in the maintenance of cooperation among rhizobia within the rhizobia-legume mutualism. In the case where the cooperative and kin recognition loci are independently inherited, spatial structure alone maintains cooperation, while kin recognition decreases the equilibrium frequency of cooperators. In the case of coinheritance, spatial structure remains a stronger force, but kin recognition can transiently increase the frequency of cooperators. Our results suggest that spatial structure can be a dominant force in maintaining cooperation in rhizobium populations, providing a mechanism for maintaining the mutualistic nodulation trait. Further, our model generates unique and testable predictions that could be evaluated empirically within the legume-rhizobium mutualism

Native Microbes Amplify Native Seedling Establishment and Diversity While Inhibiting a Non-Native Grass

Although several studies have shown increased native plant establishment with native microbe soil amendments, few studies have investigated how microbes can alter seedling recruitment and establishment in the presence of a non-native competitor. In this study, the effect of microbial communities on seedling biomass and diversity was assessed by seeding pots with both native prairie seeds and a non-native grass that commonly invades US grassland restorations, Setaria faberi. Soil in the pots was inoculated with whole soil collections from ex-arable land, late successional arbuscular mycorrhizal (AM) fungi isolated from a nearby tallgrass prairie, with both prairie AM fungi and ex-arable whole soil, or with a sterile soil (control). We hypothesized (1) late successional plants would benefit from native AM fungi, (2) that non-native plants would outcompete native plants in ex-arable soils, and (3) early successional plants would be unresponsive to microbes. Overall, native plant abundance, late successional plant abundance, and total diversity were greatest in the native AM fungi+ ex-arable soil treatment. These increases led to decreased abundance of the non-native grass S. faberi. These results highlight the importance of late successional native microbes on native seed establishment and demonstrate that microbes can be harnessed to improve both plant community diversity and resistance to invasion during the nascent stages of restoration

Ecology of Floristic Quality Assessment: testing for correlations between coefficients of conservatism, species traits and mycorrhizal responsiveness

Many plant species are limited to habitats relatively unaffected by anthropogenic disturbance, so protecting these undisturbed habitats is essential for plant conservation. Coefficients of conservatism (C values) were developed as indicators of a species’ sensitivity to anthropogenic disturbance, and these values are used in Floristic Quality Assessment as a means of assessing natural areas and ecological restoration. However, assigning of these values is subjective and improved quantitative validation of C values is needed. We tested whether there are consistent differences in life histories between species with high and low C values. To do this, we grew 54 species of tallgrass prairie plants in a greenhouse and measured traits that are associated with trade-offs on the fast-slow continuum of life-history strategies. We also grew plants with and without mycorrhizal fungi as a test of these species’ reliance on this mutualism. We compared these traits and mycorrhizal responsiveness to C values. We found that six of the nine traits we measured were correlated with C values, and together, traits predicted up to 50 % of the variation in C values. Traits including fast growth rates and greater investment in reproduction were associated with lower C values, and slow growth rates, long-lived leaves and high root:shoot ratios were associated with higher C values. Additionally, plants with high C values and a slow life history were more responsive to mutualisms with mycorrhizal fungi. Overall, our results connect C values with life-history trade-offs, indicating that high C value species tend to share a suite of traits associated with a slow life history