Dynamics and mechanisms of secondary invasion following biological control of an invasive plant.

Secondary invasions in which nontarget invaders expand following eradication of a target invader commonly occur in habitats with multiple invasive plant species and can prevent recovery of native communities. However, the dynamics and mechanisms of secondary invasion remain unclear. Here, we conducted a common garden experiment to test underlying mechanisms of secondary invasion for 14 nontarget invaders after biological control of Ambrosia artemisiifolia in two consecutive years. We found secondary invasion for all tested nontarget invaders, but secondary invasiveness (change relative to natives) varied with species and time. Specifically, secondary invasiveness depended most strongly on phylogenetic relatedness between the target and nontarget invaders in the first year with closely related nontarget invaders being most invasive. By contrast, secondary invasiveness in the second year was mostly driven by functional traits with taller nontarget invaders or those with higher specific leaf area, or smaller seeds especially invasive. Our study indicates that secondary invasion is likely to occur wherever other invasive plants co-occur with an invasive species targeted for control. Furthermore, the most problematic invaders will initially be species closely related to the target invader but then species with rapid growth and high reproduction are most likely to be more aggressive secondary invaders.

Effects of nutrient pulses on exotic species shift from positive to neutral with decreasing water availability.

Temporal fluctuation in nutrient availability generally promotes the growth of exotic plant species and has been recognized as an important driver of exotic plant invasions. However, little is known about how the impact of fluctuating nutrients on exotic species is dependent on the availability of other resources, although most ecosystems are experiencing dramatic variations in a wide variety of resources due to global change and human disturbance. Here, we explored how water availability mediates the effect of nutrient pulses on the growth of six exotic and six native plant species. We subjected individual plants of exotic and native species to well watered or water stressed conditions. For each level of water availability, we added equivalent amounts of nutrients at a constant rate, as a single large pulse, or in multiple small pulses. Under well watered conditions, nutrient pulses promoted exotic plant growth relative to nutrients supplied constantly, while they had no significant effect on natives. In contrast, under water stressed conditions, water deficiency inhibited the growth of all exotic and native species. More importantly, nutrient pulses did not increase plant growth relative to nutrients supplied constantly and these phenomena were observed for both exotic and native species. Taken together, our study shows that the impact of fluctuating nutrient availability on the growth of exotic plant species strongly depends on the variation of other resources, and that the positive effect of nutrient pulses under well watered conditions disappears under water stressed conditions. Our findings suggest that the variation in multiple resources may have complex feedback on exotic plant invasions and, therefore, it is critical to encompass multiple resources for the evaluation of fluctuating resource availability effects on exotic plant species. This will allow us to project the invasive trajectory of exotic plant species more accurately under future global change and human disturbance.

Fluctuations in resource availability shape the competitive balance among non-native plant species.

Fluctuating resource availability plays a critical role in determining non-native plant invasions through mediating the competitive balance between non-native and native species. However, the impact of fluctuating resource availability on interactions among non-native species remains largely unknown. This represents a barrier to understanding invasion mechanisms, particularly in habitats that harbor multiple non-native species with different responses to fluctuating resource availability. To examine the responses of non-native plant species to nutrient fluctuations, we compared the growth of each of 12 non-native species found to be common in local natural areas to nutrients supplied at a constant rate or supplied as a single large pulse in a pot experiment. We found that seven species produced more biomass with pulsed nutrients compared to constant nutrients (hereafter "benefitting species"), while the other five species did not differ between nutrient enrichment treatments (hereafter "non-benefitting species"). To investigate how nutrient fluctuations influence the interactions among non-native plant species, we established experimental non-native communities in the field with two benefitting and two non-benefitting non-native species. Compared with constant nutrient supply, the single large pulse of nutrient did not influence community biomass, but strongly increased the biomass and cover of the benefitting species and decreased those of the non-benefitting species. Furthermore, the benefitting species had higher leaf N content and greater plant height when nutrients were supplied as a single large pulse than at a constant rate, whereas the non-benefitting species showed no differences in leaf N content and were shorter when nutrients were supplied as a single large pulse than at a constant rate. Our results add to the growing evidence that the individual responses of non-native species to nutrient fluctuation are species-specific. More importantly, benefitting species were favored by nutrients coming in a pulse, while non-benefitting ones were favored by nutrients coming constantly when they grew together. This suggests that nutrient fluctuations can mediate the competitive balance among non-native plants and may thus determine their invasion success in a community harboring multiple non-native plant species.

Environment and geographic distance differ in relative importance for determining fungal community of rhizosphere and bulk soil.

Rhizospheric fungi play major roles in both natural and agricultural ecosystems. However, little is known about the determinants of their diversity and biogeographic patterns. Here, we compared fungal communities in rhizosphere and bulk soils of wheat fields in the North China Plain. The rhizosphere had a lower fungal diversity (observed OTUs and Chao1) than bulk soil, and a distinct fungal community structure in rhizosphere compared with bulk soil. The relative importance of environmental factors and geographic distance for fungal distribution differed between rhizosphere and bulk soil. Environmental factors were the primary cause of variations in total fungal community and major fungal phyla in bulk soil. By contrast, fungal communities in soils loosely attached to roots were predictable from both environmental factors and influences of geographic distance. Communities in soils tightly attached to roots were mainly determined by geographic distance. Our results suggest that both contemporary environment processes (present-day abiotic and biotic environment characters) and historical processes (spatial isolation, dispersal limitation occurred in the past) dominate variations of fungal communities in wheat fields, but their relative importance of all these processes depends on the proximity of fungal community to the plant roots.

Nitrogen fertilization reduces plant diversity by changing the diversity and stability of arbuscular mycorrhizal fungal community in a temperate steppe.

Nitrogen (N) deposition resulting from anthropogenic activities poses threats to ecosystem stability by reducing plant and microbial diversity. However, the role of soil microbes, particularly arbuscular mycorrhizal fungi (AMF), as mediators of N-induced shifts in plant diversity remains unclear. In this study, we conducted 6 and 11 years of N addition field experiments in a temperate steppe to investigate AMF richness and network stability and their associations with plant species richness in response to N deposition. The N fertilization, especially in the 11 years of N addition, profoundly decreased the AMF richness and plant species richness. Furthermore, N fertilization significantly decreased the AMF network complexity and stability, with these effects becoming more enhanced with the increase in N addition duration. AMF richness and network stability showed positive associations with plant diversity, and these associations were stronger after 11 than 6 years of N addition. Our findings suggest that N deposition may lead to plant diversity loss via a reduction of AMF richness and network stability, with these effects strengthened over time. This study provides a better understanding of plant-AMF interactions and their response to the prevailing global N deposition.

Foliar Herbivory Reduces Rhizosphere Fungal Diversity and Destabilizes the Co-occurrence Network.

Insect herbivores can adversely impact terrestrial plants throughout ontogeny and across various ecosystems. Simultaneously, the effects of foliar herbivory may extend belowground, to the soil microbial community. However, the responses in terms of the diversity, assembly, and stability of rhizosphere fungi to aboveground herbivory remain understudied. Here, using high-throughput sequencing, the effects of foliar insect herbivory on rhizosphere fungal microbes were investigated in a common garden experiment that manipulated herbivory intensity and time from herbivore removal. The number of observed fungal species was reduced by a greater herbivory intensity, with some species evidently sensitive to herbivory intensity and time since herbivore removal. Rhizofungal assembly processes were altered by both herbivory intensity and time since herbivore removal. Further, we found evidence that both factors strongly influenced fungal community stability: a high intensity of herbivory coupled with a shorter time since herbivore removal resulted in low stability. These results suggest that foliar herbivory can adversely alter fungal diversity and stability, which would in turn be harmful for plant health. Fortunately, the effect seems to gradually diminish with time elapsed after herbivore removal. Our findings provide a fresh, in-depth view into the roles of rhizofungi in enhancing the adaption ability of plants under environmental stress.

Microbes changed their carbon use strategy to regulate the priming effect in an 11-year nitrogen addition experiment in grassland.

Nitrogen availability is a key factor that regulates soil priming (the strong short-term changes in microbial decomposition of soil organic carbon after addition of fresh carbon resources); however, how soil priming changes under nitrogen addition is unclear. In this study, we collected soils from a grassland with 11-year history of nitrogen addition (0, 60, 120, and 240 kg N ha-1 yr-1 NH4NO3), and the soils were incubated for 6 weeks to estimate the direction and magnitude of soil priming and the underlying microbial carbon use strategy. We found glucose addition triggered a positive priming effect among all the treatments; however, the magnitude of the positive priming did not change under nitrogen addition. The stable soil organic carbon content under different nitrogen addition levels might support the no significant change in the magnitude of those positive priming. Using DNA stable-isotope probing (DNA-SIP), we found that bacterial and fungal taxa consuming the added glucose were different in different nitrogen addition levels. The relative abundance of the K-strategist Acidobacteria increased with increasing nitrogen addition levels, while the r-strategist Firmicutes decreased with increasing nitrogen addition levels. Our results indicated microbial taxa exhibited carbon use plasticity, with most taxa altering their use of glucose under nitrogen addition.

Space Is More Important than Season when Shaping Soil Microbial Communities at a Large Spatial Scale.

The relative importance of spatial and temporal variability in shaping the distribution of soil microbial communities at a large spatial scale remains poorly understood. Here, we explored the relative importance of space versus time when predicting the distribution of soil bacterial and fungal communities across North China Plain in two contrasting seasons (summer versus winter). Although we found that microbial alpha (number of phylotypes) and beta (changes in community composition) diversities differed significantly between summer and winter, space rather than season explained more of the spatiotemporal variation of soil microbial alpha and beta diversities. Environmental covariates explained some of microbial spatiotemporal variation observed, with fast-changing environmental covariates-climate variables, soil moisture, and available nutrient-likely being the main factors that drove the seasonal variation found in bacterial and fungal beta diversities. Using random forest modeling, we further identified a group of microbial exact sequence variants (ESVs) as indicators of summer and winter seasons and for which relative abundance was associated with fast-changing environmental variables (e.g., soil moisture and dissolved organic nitrogen). Together, our empirical field study's results suggest soil microbial seasonal variation could arise from the changes of fast-changing environmental variables, thus providing integral support to the large emerging body of snapshot studies related to microbial biogeography.IMPORTANCE Both space and time are key factors that regulate microbial community, but microbial temporal variation is often ignored at a large spatial scale. In this study, we compared spatial and seasonal effects on bacterial and fungal diversity variation across an 878-km transect and found direct evidence that space is far more important than season in regulating the soil microbial community. Partitioning the effect of season, space and environmental variables on microbial community, we further found that fast-changing environmental factors contributed to microbial temporal variation.

Interannual climate variability and altered precipitation influence the soil microbial community structure in a Tibetan Plateau grassland.

Climate change could influence aboveground and belowground plant community diversity and structure profoundly. However, our understanding of the responses of microbial communities to changes in both temperature and precipitation remains poor. Here, using 16S rDNA and ITS high throughput sequencing, we investigated the responses of soil bacterial and fungal community structure to both temperature and precipitation changes, and how such changes could influence interannual variability within soil microbial communities in a grassland in the Tibetan Plateau. The altered precipitation treatments had significant effects on soil bacterial and fungal community structure (F = 2.11, P = 0,001; F = 2.26. P = 0.001, respectively), while year had a more significant effect on soil bacterial and fungal community structure (F = 3.36, P = 0.001; F = 2.67, P = 0.001, respectively). The results showed that the interannual fluctuations in mean annual precipitation and mean annual temperature were significantly correlated with the interannual variations in soil bacterial and fungal community structures. In addition, the robustness of co-occurrence relationships among microbes could be strongly influenced by the altered precipitation and year. Overall, our results indicated that the effect of interannual climate variability on the soil microbial community was greater than the effect of a 1.6 °C increase in temperature. Our findings suggest an interactive effect of rapid interannual variability and slow climate change on the belowground soil microbial community structure.

Salinity Is a Key Determinant for Soil Microbial Communities in a Desert Ecosystem.

Soil salinization is a growing environmental problem caused by both natural and human activities. Excessive salinity in soil suppresses growth, decreases species diversity, and alters the community composition of plants; however, the effect of salinity on soil microbial communities is poorly understood. Here, we characterize the soil microbial community along a natural salinity gradient in Gurbantunggut Desert, Northwestern China. Microbial diversity linearly decreased with increases in salinity, and community dissimilarity significantly increased with salinity differences. Soil salinity showed a strong effect on microbial community dissimilarity, even after controlling for the effects of spatial distance and other environmental variables. Microbial phylotypes (n = 270) belonging to Halobacteria, Nitriliruptoria, [Rhodothermi], Gammaproteobacteria, and Alphaproteobacteria showed a high-salinity niche preference. Out of nine potential phenotypes predicted by BugBase, oxygen-related phenotypes showed a significant relationship with salinity content. To explore the community assembly processes, we used null models of within-community (nearest-taxon index [NTI]) and between-community (ßNTI) phylogenetic composition. NTI showed a significantly negative relationship with salinity, suggesting that the microbial community was less phylogenetically clustered in more-saline soils. ßNTI, the between-community analogue of NTI, showed that deterministic processes have overtaken stochastic processes across all sites, suggesting the importance of environmental filtering in microbial community assembly. Taken together, these results suggest the importance of salinity in soil microbial community composition and assembly processes in a desert ecosystem. IMPORTANCE Belowground microorganisms are indispensable components for nutrient cycling in desert ecosystems, and understanding how they respond to increased salinity is essential for managing and ameliorating salinization. Our sequence-based data revealed that microbial diversity decreased with increasing salinity, and certain salt-tolerant phylotypes and phenotypes showed a positive relationship with salinity. Using a null modeling approach to estimate microbial community assembly processes along a salinity gradient, we found that salinity imposed a strong selection pressure on the microbial community, which resulted in a dominance of deterministic processes. Studying microbial diversity and community assembly processes along salinity gradients is essential in understanding the fundamental ecological processes in desert ecosystems affected by salinization.

Fungal Communities Along a Small-Scale Elevational Gradient in an Alpine Tundra Are Determined by Soil Carbon Nitrogen Ratios.

Elevational gradients are associated not only with variations in temperature and precipitation, but also with shifts in vegetation types and changes in soil physicochemical properties. While large-scale elevational patterns of soil microbial diversity, such as monotonic declines and hump-shaped models, have been reported, it is unclear whether within-ecosystem elevational distribution patterns exist for soil fungal communities at the small scale. Using Illumina Miseq DNA sequencing, we present a comprehensive analysis of soil fungal diversity and community compositions in an alpine tundra ecosystem at elevations ranging from 2000 to 2500 m on the Changbai Mountain, China. Soil fungal community composition differed among elevations, and the fungal diversity (i.e., species richness and Chao1) increased along elevations. Soil fungal richness was negatively correlated with soil carbon/nitrogen (C/N) ratio, and community composition varied according to the C/N ratio. In addition, the relative abundances of Basidiomycota and Leotiomycetes were similarly negatively correlated with C/N ratio. For functional guilds, our data showed that mycoparasite and foliar epiphyte abundances were also influenced by C/N ratio. These results indicated that soil C/N ratio might be a key factor in determining soil fungal distribution at small-scale elevational gradients.

Spatial scale affects the relative role of stochasticity versus determinism in soil bacterial communities in wheat fields across the North China Plain.

BACKGROUND: The relative importance of stochasticity versus determinism in soil bacterial communities is unclear, as are the possible influences that alter the balance between these. Here, we investigated the influence of spatial scale on the relative role of stochasticity and determinism in agricultural monocultures consisting only of wheat, thereby minimizing the influence of differences in plant species cover and in cultivation/disturbance regime, extending across a wide range of soils and climates of the North China Plain (NCP). We sampled 243 sites across 1092 km and sequenced the 16S rRNA bacterial gene using MiSeq. We hypothesized that determinism would play a relatively stronger role at the broadest scales, due to the strong influence of climate and soil differences in selecting many distinct OTUs of bacteria adapted to the different environments. In order to test the more general applicability of the hypothesis, we also compared with a natural ecosystem on the Tibetan Plateau. RESULTS: Our results revealed that the relative importance of stochasticity vs. determinism did vary with spatial scale, in the direction predicted. On the North China Plain, stochasticity played a dominant role from 150 to 900 km (separation between pairs of sites) and determinism dominated at more than 900 km (broad scale). On the Tibetan Plateau, determinism played a dominant role from 130 to 1200 km and stochasticity dominated at less than 130 km. Among the identifiable deterministic factors, soil pH showed the strongest influence on soil bacterial community structure and diversity across the North China Plain. Together, 23.9% of variation in soil microbial community composition could be explained, with environmental factors accounting for 19.7% and spatial parameters 4.1%. CONCLUSIONS: Our findings revealed that (1) stochastic processes are relatively more important on the North China Plain, while deterministic processes are more important on the Tibetan Plateau; (2) soil pH was the major factor in shaping soil bacterial community structure of the North China Plain; and (3) most variation in soil microbial community composition could not be explained with existing environmental and spatial factors. Further studies are needed to dissect the influence of stochastic factors (e.g., mutations or extinctions) on soil microbial community distribution, which might make it easier to predictably manipulate the microbial community to produce better yield and soil sustainability outcomes.

Corrigendum: Effects of Short-Term Warming and Altered Precipitation on Soil Microbial Communities in Alpine Grassland of the Tibetan Plateau.

[This corrects the article on p. 1032 in vol. 7, PMID: 27446064.].

Effects of Short-Term Warming and Altered Precipitation on Soil Microbial Communities in Alpine Grassland of the Tibetan Plateau.

Soil microbial communities are influenced by climate change drivers such as warming and altered precipitation. These changes create abiotic stresses, including desiccation and nutrient limitation, which act on microbes. However, our understanding of the responses of microbial communities to co-occurring climate change drivers is limited. We surveyed soil bacterial and fungal diversity and composition after a 1-year warming and altered precipitation manipulation in the Tibetan plateau alpine grassland. In isolation, warming and decreased precipitation treatments each had no significant effects on soil bacterial community structure; however, in combination of both treatments altered bacterial community structure (p = 0.03). The main effect of altered precipitation specifically impacted the relative abundances of Bacteroidetes and Gammaproteobacteria compared to the control, while the main effect of warming impacted the relative abundance of Betaproteobacteria. In contrast, the fungal community had no significant response to the treatments after 1-year. Using structural equation modeling (SEM), we found bacterial community composition was positively related to soil moisture. Our results indicate that short-term climate change could cause changes in soil bacterial community through taxonomic shifts. Our work provides new insights into immediate soil microbial responses to short-term stressors acting on an ecosystem that is particularly sensitive to global climate change.