Sarah M. Emery

Fungal symbionts alter plant responses to global change

While direct plant responses to global change have been well characterized, indirect plant responses to global change, via altered species interactions, have received less attention. Here, we examined how plants associated with four classes of fungal symbionts (class I leaf endophytes [EF], arbuscular mycorrhizal fungi [AMF], ectomycorrhizal fungi [ECM], and dark septate endophytes [DSE]) responded to four global change factors (enriched CO2, drought, N deposition, and warming). We performed a meta-analysis of 434 studies spanning 174 publications to search for generalizable trends in responses of plant-fungal symbioses to future environments. Specifically, we addressed the following questions: (1) Can fungal symbionts ameliorate responses of plants to global change? (2) Do fungal symbiont groups differ in the degree to which they modify plant response to global change? (3) Do particular global change factors affect plant-fungal symbioses more than others? In all global change scenarios, except elevated CO2, fungal symbionts significantly altered plant responses to global change. In most cases, fungal symbionts increased plant biomass in response to global change. However, increased N deposition reduced the benefits of symbiosis. Of the global change factors we considered, drought and N deposition resulted in the strongest fungal mediation of plant responses. Our analysis highlighted gaps in current knowledge for responses of particular fungal groups and revealed the importance of considering not only the nonadditive effects of multiple global change factors, but also the interactive effects of multiple fungal symbioses. Our results show that considering plant-fungal symbioses is critical to predicting ecosystem response to global change.

Dominant species identity, not community evenness, regulates invasion in experimental grassland plant communities.

While there has been extensive interest in understanding the relationship between diversity and invasibility of communities, most studies have only focused on one component of diversity: species richness. Although the number of species can affect community invasibility, other aspects of diversity, including species identity and community evenness, may be equally important. While several field studies have examined how invasibility varies with diversity by manipulating species identity or evenness, the results are often confounded by resource heterogeneity, site history, or disturbance. We designed a mesocosm experiment to examine explicitly the role of dominant species identity and evenness on the invasibility of grassland plant communities. We found that the identity of the dominant plant species, but not community evenness, significantly impacted invasibility. Using path analysis, we found that community composition (dominant species identity) reduced invasion by reducing early-season light availability and increasing late-season plant community biomass. Nitrogen availability was an important factor for the survival of invaders in the second year of the experiment. We also found significant direct effects of certain dominant species on invasion, although the mechanisms driving these effects remain unclear. The magnitude of dominant species effects on invasibility we observed are comparable to species richness effects observed in other studies, showing that species composition and dominant species can have strong effects on the invasibility of a community.

Generality in ecology: testing North American grassland rules in South African savannas

Ecology has emerged as a global science, and there is a pressing need to identify ecological rules – general principles that will improve its predictive capability for scientists and its usefulness for managers and policy makers. Ideally, the generality and limits of these ecological rules should be assessed using extensive, coordinated experiments that ensure consistency in design and comparability of data. To improve the design of these large-scale efforts, existing data should be used to test prospective ecological rules and to identify their limits and contingencies. As an example of this approach, we describe prospective rules for grassland responses to fire and rainfall gradients, identified from long-term studies of North American grasslands and tested with existing data from long-term experiments in South African savanna grasslands. Analyses indicated consistent effects of fire on the abundance of the dominant (grasses) and subdominant (forbs) flora on both continents, but no common response of gr...

Pollinator Visits to Threatened Species Are Restored Following Invasive Plant Removal

An indirect consequence of plant invasions is the disruption of native plant-pollinator interactions. We examined effects of invasive baby’s breath (Gypsophila paniculata) and spotted knapweed (Centaurea maculosa) on floral visitors to federally threatened Pitcher’s thistle (Cirsium pitcheri) in Lake Michigan dunes. In sweep net surveys, abundances of pollinator taxa were five times higher in invaded than in naturally invader-free sites. However, plot-level G. paniculata removal treatments increased pollinator visits to C. pitcheri relative to invaded plots and restored visitation to levels found in naturally uninvaded plots. Invader removal also increased native plant species richness, which was positively correlated with pollinator visitation to C. pitcheri, suggesting an indirect effect on pollinators mediated through invader-altered plant composition. In temporary floral arrays, the rate of pollinator visitation to C. pitcheri was not affected by neighbor plant species identity. However, compared with native Monarda punctata, invasive C. maculosa attracted more total pollinators to the array but reduced the proportion of total visits that were to C. pitcheri and increased pollinator movements between plant species. While both G. paniculata and C. maculosa appear to act as magnet species by attracting more pollinators at the plot level, these invaders have the potential to reduce reproduction of C. pitcheri by decreasing pollinator visits and increasing interspecific pollen transfer.

Variation in Endophyte Symbiosis, Herbivory and Drought Tolerance of Ammophila breviligulata Populations in the Great Lakes Region

Abstract Ecologists have come to appreciate that plant genotype can affect the success of restoration efforts, but the role of plant symbionts has received less attention. Epichloë-type endophytic fungi (EF) grow in the aboveground tissues of most plants and occur systemically in 20–30% of all grass species. Despite the potential for EF to alter plant competitive hierarchies and to be lost under improper seed storage, they have yet to be considered as an important factor in plant restoration ecology. We surveyed EF infection frequency in 42 native and restored populations of the dominant Great Lakes dune grass Ammophila breviligulata. We also conducted a greenhouse experiment to compare effects of herbivory and drought on an uninfected Michigan population of A. breviligulata and the commercially available ‘Cape’ variety, which is commonly planted for restoration. Surveys revealed low levels of EF infection in natural populations in the Great Lakes region. ‘Cape’ nursery stock was 100% infected. In the greenhouse, the Michigan plants were more sensitive to grasshopper herbivory and drought than the ‘Cape’ plants. Our results suggest that the variety of A. breviligulata used in dune restorations possibly could alter plant and insect community dynamics due to differences in EF status, though further tests under field conditions are needed.

Biotic and abiotic predictors of ecosystem engineering traits of the dune building grass, Ammophila breviligulata

Ecosystem engineers are species that fundamentally influence their community and ecosystem by creating or altering the physical structure of habitats. However, the function of ecosystem engineers is variable and can depend on abiotic and biotic factors. In this study, we characterized the ecosystem engineering traits of plant size and tiller density for the dune grass, Ammophila breviligulata, in 37 sites across a broad geographic gradient in the western Great Lakes region. We also measured 20 biotic and abiotic factors related to climate, soil chemistry, and fungal symbionts associated with these survey sites and assessed their relationships with A. breviligulata population traits and dune plant species richness. Climate factors, especially temperature and precipitation, were positively associated with A. breviligulata tiller size, while soil organic matter was the only factor associated with tiller density. Several factors, including temperature, soil nitrogen, and mycorrhizal colonization, were associated with plant richness across our sites. Our results suggest that climate can influence at least some ecosystem engineering traits (i.e., plant size) of an important dune building species, although general conclusions from our work indicate that the population trait tied most closely with dune building ability—population density—is not strongly influenced by climate at the regional scale. This offers insight for conservationists interested in preserving intact dune ecosystems in a changing climate, but further work is needed to reconcile conflicting lab and field studies.

Impact of Competition and Mycorrhizal Fungi on Growth of Centaurea stoebe, an Invasive Plant of Sand Dunes

Abstract Soil biota such as arbuscular mycorrhizal fungi (AMF) have been shown to increase invasive plant species success in a wide variety of systems by providing both direct and indirect benefits to the invader. For example, Centaurea stoebe invasion in the western US is at least partially due to AMF networks allowing Centaurea to parasitize some native plant species. Centaurea also invades sand dune systems of the northern Great Lakes region, which often have reduced or altered soil communities compared to other grasslands. In these habitats, AMF may play a different role in invasion success of this species. We conducted a greenhouse experiment to compare effects of soil biota and AMF on competitive interactions between Centaurea and two varieties of Ammophila breviligulata, a dominant native grass of Great Lakes sand dunes. We found that Centaurea growth was slowed by the presence of Ammophila competitors, while AMF had no direct or indirect effect on growth. Both Ammophila varieties were uninhibited by the presence of Centaurea. The commercially available Cape variety of Ammophila had more than twice the inhibitory effect of a native Michigan variety on Centaurea growth. It does not appear that Centaurea takes advantage of AMF networks in this dune system. Indeed, since Centaurea growth is actually reduced in direct competition with Ammophila, we suspect that invasion of dunes by this species is a result of disturbance. For land managers, planting Ammophila in open areas as part of a restoration plan may slow spread of Centaurea in this system.

Fungal symbiosis and precipitation alter traits and dune building by the ecosystem engineer, Ammophila breviligulata

Ecosystem engineer species influence their community and ecosystem by creating or altering the physical structure of habitats. The function of ecosystem engineers is variable and can depend on both abiotic and biotic factors. Here we make use of a primary successional system to evaluate the direct and interactive effects of climate change (precipitation) and fungal endophyte symbiosis on population traits and ecosystem function of the ecosystem engineering grass species, Ammophila breviligulata. We manipulated endophyte presence in A. breviligulata in combination with rain-out shelters and rainfall additions in a factorial field experiment established in 2010 on Lake Michigan sand dunes. We monitored plant traits, survival, growth, and sexual reproduction of A. breviligulata from 2010-2013, and quantified ecosystem engineering as the sand accumulation rate. Presence of the endophyte in A. breviligulata increased vegetative growth by up to 19%, and reduced sexual reproduction by up to 46% across all precipitation treatments. Precipitation was a less significant factor than endophyte colonization for A. breviligulata growth. Reduced precipitation increased average leaf number per tiller but had no other effects on plant traits. Changes in A. breviligulata traits corresponded to increases in sand accumulation in plots with the endophyte as well as in plots with reduced precipitation. Sand accumulation is a key ecosystem function in these primary successional habitats, and so microbial symbiosis in this ecosystem engineer could lead to direct effects on the value of these dune habitats for humans.

The showy invasive plant Ranunculus ficaria facilitates pollinator activity, pollen deposition, but not always seed production for two native spring ephemeral plants

Showy invasive plants can reduce pollinator visitation to native plants, resulting in a reduction of seed-set in insect-pollinated species. Seed set in native plants may also be reduced due to the presence of foreign pollen. Alternatively, additional floral resources provided by invasive plants may increase pollinator activity, and facilitate pollination of native species. Ranunculus ficaria is a perennial herb invading deciduous forests of the eastern United States. It produces many showy flowers that may influence pollinator activity in heavily invaded habitats. We compared pollinator visitation rates, stigma pollen loads, and seed production of two sympatrically flowering, entomophilous native species (Claytonia virginica and Cardamine concatenata) between habitats invaded by R. ficaria and uninvaded habitats. We found significantly higher pollinator activity (visits to plots) in invaded plots. We also found significantly higher per flower visitation rates to C. virginica in invaded plots. Claytonia virginica stigmas from invaded habitats had more conspecific pollen resulting in more seeds per capsule in invaded areas. There was more conspecific pollen on C. concatenata stigmas in invaded compared to uninvaded habitats, but there were significantly more seeds per silique in uninvaded habitats. Our results indicated that this invasive species increases pollinator activity and conspecific pollen deposition on sympatrically flowering native ephemerals, but may have differential effects on native seed production. Management options should consider the facilitative effects of this species on pollination services, as well as the possible negative competitive effects.

Fire and non‐native grass invasion interact to suppress tree regeneration in temperate deciduous forests

Summary 1. While many ecosystems depend on fire to maintain biodiversity, non-native plant invasions can enhance fire intensity, suppressing native species and generating a fire–invasion feedback. These dynamics have been observed in arid and semi-arid ecosystems, but fire–invasion interactions in temperate deciduous forests, where prescribed fires are often used as management tools to enhance native diversity, have rarely been investigated. 2. Here we evaluated the effects of a widespread invasive grass on fire behaviour in eastern deciduous forests in the USA and the potential effects of fire and invasions on tree regeneration. We planted native trees into invaded and uninvaded forests, quantified fuel loads, then applied landscape-scale prescribed fires and no-burn controls, and measured fire behaviour and tree seedling and invasive plant performance. 3. Our results show that fires in invaded habitats were significantly more intense, including higher fire temperatures, longer duration and higher flame heights, even though invasions did not alter total fuel loads. The invasion plus fire treatment suppressed native tree seedling survival by 54% compared to invasions without fire, and invasions reduced natural tree recruitment by 66%. 4. We also show that invasive plant biomass did not change from one season to the next in plots where fire was applied, but invader biomass declined significantly in unburned reference plots, suggesting a positive invasive grass–fire feedback. 5. Synthesis and applications. These findings demonstrate that fire–invasion interactions can have significant consequences for invaded temperate forest ecosystems by increasing fire intensity and reducing tree establishment while promoting invasive plant persistence. To encourage tree regeneration and slow invasive spread, we recommend that forest managers remove invasions prior to applying prescribed fires or avoid the use of fire in habitats invaded by non-native grasses.