Invasive Grass Dominance over Native Forbs Is Linked to Shifts in the Bacterial Rhizosphere Microbiome.

Rhizosphere microbiomes have received growing attention in recent years for their role in plant health, stress tolerance, soil nutrition, and invasion. Still, relatively little is known about how these microbial communities are altered under plant competition, and even less about whether these shifts are tied to competitive outcomes between native and invasive plants. We investigated the structure and diversity of rhizosphere bacterial and fungal microbiomes of native annual forbs and invasive annual grasses grown in a shade-house both individually and in competition using high-throughput amplicon sequencing of the bacterial 16S rRNA gene and the fungal ITS region. We assessed how differentially abundant microbial families correlate to plant biomass under competition. We find that bacterial diversity and structure differ between native forbs and invasive grasses, but fungal diversity and structure do not. Furthermore, bacterial community structures under competition are distinct from individual bacterial community structures. We also identified five bacterial families that varied in normalized abundance between treatments and that were correlated with plant biomass under competition. We speculate that invasive grass dominance over these natives may be partially due to effects on the rhizosphere community, with changes in specific bacterial families potentially benefiting invaders at the expense of natives.

Invasive species interact with climatic variability to reduce success of natives.

Plants have evolved resource-conservative and resource-acquisitive strategies to deal with variability in rainfall, but interactions with dominant invasive species may undermine these adaptations. To investigate the relative effect of invaders on species with these two strategies, we manipulated rainfall and invasive grass presence and measured demographic rates in three resource-acquisitive and three resource-conservative native annual forbs. We found that invasive grasses were harmful to all of the target species, but especially the resource-acquisitive ones, and that these effects were stronger under experimental drought. Invasive grass presence under drought lowered per capita population growth rates of acquisitive natives through increased mortality and decreased seed set. While invasive grasses also decreased per capita growth rates of resource-conservative natives, they did so by increasing mortality under experimental watering and by limiting the production of seed under experimental drought. Invasive species can thus interact with climatic fluctuations to make bad years worse for resource-acquisitive natives and good years less good for resource-conservative natives, and they may generally tend to undermine the acquisitive strategy more than the conservative one.

Seedling traits predict drought-induced mortality linked to diversity loss.

Trait-based approaches are increasingly used to predict ecological consequences of climate change, yet seldom have solid links been established between plant traits and observed climate-driven community changes. Most analyses have focused on aboveground adult plant traits, but in warming and drying climates, root traits may be critical, and seedlings may be the vulnerable stage. Relationships of seedling and root traits to more commonly measured traits and ecological outcomes are poorly known. In an annual grassland where winter drought-induced seedling mortality is driving a long-term decline in native diversity, using a field experiment during the exceptionally dry winter of 2017-2018, we found that seedling mortality was higher and growth of seedlings and adults were lower in unwatered than watered sites. Mortality of unwatered seedlings was higher in species with shorter seedling roots, and also in species with the correlated traits of small seeds, high seedling specific leaf area (SLA), and tall seedlings. Adult traits varied along an axis from short-stature, high SLA and foliar N, and early flowering to the opposite values, and were only weakly correlated with seedling traits and seedling mortality. No evidence was found for adaptive plasticity, such as longer roots or lower SLA in unwatered plants. Among these species, constitutive variation in seedling root length explained most of the variation in survival of a highly vulnerable life stage under winter drought. Selective loss of species with high adult SLA, observed in this community and others under drought stress, may be the byproduct of other correlated traits.

Seed banks of native forbs, but not exotic grasses, increase during extreme drought.

Extreme droughts such as the one that affected California in 2012-2015 have been linked to severe ecological consequences in perennial-dominated communities such as forests. In annual communities, drought impacts are difficult to assess because many species persist through facultative multiyear seed dormancy, which leads to the development of seed banks. Impacts of extreme drought on the abundance and composition of the seed banks of whole communities are little known. In 80 heterogeneous grassland plots where cover is dominated by ~15 species of exotic annual grasses and diversity is dominated by ~70 species of native annual forbs, we grew out seeds from soil cores collected early in the California drought (2012) and later in the multiyear drought (2014), and analyzed drought-associated changes in the seed bank. Over the course of the study we identified more than 22,000 seedlings to species. We found that seeds of exotic annual grasses declined sharply in abundance during the drought while seeds of native annual forbs increased, a pattern that resembled but was even stronger than the changes in aboveground cover of these groups. Consistent with the expectation that low specific leaf area (SLA) is an indicator of drought tolerance, we found that the community-weighted mean SLA of annual forbs declined both in the seed bank and in the aboveground community, as low-SLA forbs increased disproportionately. In this system, seed dormancy reinforces the indirect benefits of extreme drought to the native forb community.

Climate-driven diversity change in annual grasslands: Drought plus deluge does not equal normal.

Climate forecasts agree that increased variability and extremes will tend to reduce the availability of water in many terrestrial ecosystems. Increasingly severe droughts may be exacerbated both by warmer temperatures and by the relative unavailability of water that arrives in more sporadic and intense rainfall events. Using long-term data and an experimental water manipulation, we examined the resilience of a heterogeneous annual grassland community to a prolonged series of dry winters that led to a decline in plant species richness (2000-2014), followed by a near-record wet winter (2016-2017), a climatic sequence that broadly resembles the predicted future in its high variability. In our 80, 5-m2 observational plots, species richness did not recover in response to the wet winter, and the positive relationship of richness to annual winter rainfall thus showed a significant weakening trend over the 18-year time period. In experiments on 100, 1-m2 plots, wintertime water supplementation increased and drought shelters decreased the seedling survival and final individual biomass of native annual forbs, the main functional group contributing to the observed long-term decline in richness. Water supplementation also increased the total cover of native annual forbs, but only increased richness within nested subplots to which seeds were also added. We conclude that prolonged dry winters, by increasing seedling mortality and reducing growth of native forbs, may have diminished the seedbank and thus the recovery potential of diversity in this community. However, the wet winter and the watering treatment did cause recovery of the community mean values of a key functional trait (specific leaf area, an indicator of drought intolerance), suggesting that some aggregate community properties may be stabilized by functional redundancy among species.

Positive interactions between herbivores and plant diversity shape forest regeneration.

The effects of herbivores and diversity on plant communities have been studied separately but rarely in combination. We conducted two concurrent experiments over 3 years to examine how tree seedling diversity, density and herbivory affected forest regeneration. One experiment factorially manipulated plant diversity (one versus 15 species) and the presence/absence of deer (Odocoileus virginianus). We found that mixtures outperformed monocultures only in the presence of deer. Selective browsing on competitive dominants and associational protection from less palatable species appear responsible for this herbivore-driven diversity effect. The other experiment manipulated monospecific plant density and found little evidence for negative density dependence. Combined, these experiments suggest that the higher performance in mixture was owing to the acquisition of positive interspecific interactions rather than the loss of negative intraspecific interactions. Overall, we emphasize that realistic predictions about the consequences of changing biodiversity will require a deeper understanding of the interaction between plant diversity and higher trophic levels. If we had manipulated only plant diversity, we would have missed an important positive interaction across trophic levels: diverse seedling communities better resist herbivores, and herbivores help to maintain seedling diversity.