Habitats Within the Plant Root Differ in Bacterial Network Topology and Taxonomic Assortativity.

The root microbiome is composed of distinct epiphytic (rhizosphere) and endophytic (endosphere) habitats. Differences in abiotic and biotic factors drive differences in microbial community diversity and composition between these habitats, though how they shape the interactions among community members is unknown. Here, we coupled a large-scale characterization of the rhizosphere and endosphere bacterial communities of 30 plant species across two watering treatments with co-occurrence network analysis to understand how root habitats and soil moisture shape root bacterial network properties. We used a novel bootstrapping procedure and null network modeling to overcome some of the limitations associated with microbial co-occurrence network construction and analysis. Endosphere networks had elevated node betweenness centrality versus the rhizosphere, indicating greater overall connectivity among core bacterial members of the root endosphere. Taxonomic assortativity was higher in the endosphere, whereby positive co-occurrence was more likely between bacteria within the same phylum while negative co-occurrence was more likely between bacterial taxa from different phyla. This taxonomic assortativity could be driven by positive and negative interactions among members of the same or different phylum, respectively, or by similar niche preferences associated with phylum rank among root inhabiting bacteria across plant host species. In contrast to the large differences between root habitats, drought had limited effects on network properties but did result in a higher proportion of shared co-occurrences between rhizosphere and endosphere networks. Our study points to fundamentally different ecological processes shaping bacterial co-occurrence across root habitats. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Assembly and ecological function of the root microbiome across angiosperm plant species.

Across plants and animals, host-associated microbial communities play fundamental roles in host nutrition, development, and immunity. The factors that shape host-microbiome interactions are poorly understood, yet essential for understanding the evolution and ecology of these symbioses. Plant roots assemble two distinct microbial compartments from surrounding soil: the rhizosphere (microbes surrounding roots) and the endosphere (microbes within roots). Root-associated microbes were key for the evolution of land plants and underlie fundamental ecosystem processes. However, it is largely unknown how plant evolution has shaped root microbial communities, and in turn, how these microbes affect plant ecology, such as the ability to mitigate biotic and abiotic stressors. Here we show that variation among 30 angiosperm species, which have diverged for up to 140 million years, affects root bacterial diversity and composition. Greater similarity in root microbiomes between hosts leads to negative effects on plant performance through soil feedback, with specific microbial taxa in the endosphere and rhizosphere potentially affecting competitive interactions among plant species. Drought also shifts the composition of root microbiomes, most notably by increasing the relative abundance of the Actinobacteria. However, this drought response varies across host plant species, and host-specific changes in the relative abundance of endosphere Streptomyces are associated with host drought tolerance. Our results emphasize the causes of variation in root microbiomes and their ecological importance for plant performance in response to biotic and abiotic stressors.

Soil-mediated impacts of an invasive thistle inhibit the recruitment of certain native plants.

Invasive plants may outcompete and replace native plant species through a variety of mechanisms. Recent evidence indicates that soil microbial pathways such as pathogen accumulation may have a considerable role in facilitating competition between native and invasive plants. To assess microbe-mediated pathways of invasion, we tested the impacts of invaded and non-invaded field soils on plant establishment using naturally occurring populations of the common Eurasian invader Cirsium arvense (Canada thistle) in Southern Ontario, Canada. Linked field and greenhouse experiments were used to quantify differences in the germinability and early growth rates of native plant species, depending on exposure to the microbial community in invaded or non-invaded soils. The invaded microbial community significantly reduced early growth rates for two of the seven native species surveyed, and decreased seed germination for another. In contrast, the germination and growth of invasive Cirsium were not affected by its own soil microbial community. These results demonstrate that the invasion of C. arvense can reduce the performance of some native plant species through changes to the soil microbial community. Different effects on different species suggest that this invader may also change the relative importance of certain natives in the invaded community. If these effects influence plant abundance in the field, microbially mediated interactions in the soil may aid the invasion of C. arvense and facilitate the disruption of invaded communities.

Does local isolation allow an invasive thistle to escape enemy pressure?

Enemy release often is invoked to explain the success of invasive plants: an invader benefits from reduced attack as it escapes specialized enemies through the invasion process. Enemy release typically is thought of as occurring at large geographic scales, but local-scale interactions may also be important for invader establishment and success. Furthermore, most tests of local enemy release have been conducted over a single year even though release may be a transient phenomenon, especially at small scales. In this study, we used a multi-year field experiment to investigate whether locally isolated populations of the noxious non-native weed Cirsium arvense benefit from reduced levels of aboveground damage, and whether any initial advantage is lost over subsequent growing seasons. Populations of C. arvense were grown in plots at set distances from established source populations for 4 years. In the first year of the experiment, folivory significantly declined with host isolation, but damage from specialist stem gallers and seed predators did not. However, in subsequent years of observation, folivores began colonizing isolated C. arvense populations while stem gallers exhibited very slow colonization of more isolated plots; seed predation showed no pattern with distance in any year. Local enemy escape did not result in increased plant performance, which instead negatively correlated with degree of isolation. Nonetheless, our results stress the importance of multi-year observations in tests of enemy release, since the herbivory patterns initially observed often changed within subsequent years depending on the dispersal ability and biology of the causal organism involved.

Phylogenetic structure predicts capitular damage to Asteraceae better than origin or phylogenetic distance to natives.

Exotic species more closely related to native species may be more susceptible to attack by native natural enemies, if host use is phylogenetically conserved. Where this is the case, the use of phylogenies that include co-occurring native and exotic species may help to explain interspecific variation in damage. In this study, we measured damage caused by pre-dispersal seed predators to common native and exotic plants in the family Asteraceae. Damage was then mapped onto a community phylogeny of this family. We tested the predictions that damage is phylogenetically structured, that exotic plants experience lower damage than native species after controlling for this structure, and that phylogenetically novel exotic species would experience lower damage. Consistent with our first prediction, 63% of the variability in damage was phylogenetically structured. When this structure was accounted for, exotic plants experienced significantly lower damage than native plants, but species origin only accounted for 3% of the variability of capitular damage. Finally, there was no support for the phylogenetic novelty prediction. These results suggest that interactions between exotic plants and their seed predators may be strongly influenced by their phylogenetic position, but not by their relationship to locally co-occurring native species. In addition, the influence of a species' origin on the damage it experiences often may be small relative to phylogenetically conserved traits.

The effects of disturbance and enemy exclusion on performance of an invasive species, common ragweed, in its native range.

Common ragweed (Ambrosia artemisiifolia) is an abundant weed in its native North America, despite supporting a wide range of natural enemies. Here, we tested whether these enemies have significant impacts on the performance of this plant in its native range. We excluded enemies from the three principal life-history stages (seed, seedling, and adult) of this annual in a series of field experiments; at the adult stage, we also manipulated soil disturbance and conspecific density. We then measured the consequences of these treatments for growth, survival, and reproduction. Excluding fungi and vertebrate granivores from seeds on the soil surface did not increase germination relative to control plots. Seedling survivorship was only slightly increased by the exclusion of molluscs and other herbivores. Insecticide reduced damage to leaves of adult plants, but did not improve growth or reproduction. Growth and survivorship of adults were strongly increased by disturbance, while higher conspecific density reduced performance in disturbed plots. These results indicate ragweed is insensitive to attack by many of its natural enemies, helping to explain its native-range success. In addition, they suggest that even though ragweed lost most of its insect folivores while invading Europe, escape from these enemies is unlikely to have provided a significant demographic advantage; instead, disturbance is likely to have been a much more important factor in its invasion. Escape from enemies should not be assumed to explain the success of exotic species unless improved performance also can be demonstrated; native-range studies can help achieve this goal.

Evidence that phylogenetically novel non-indigenous plants experience less herbivory.

The degree to which biotic interactions influence invasion by non-indigenous species may be partly explained by the evolutionary relationship of these invaders with natives. Darwin's naturalization hypothesis controversially proposes that non-native plants are more likely to invade if they lack close relatives in their new range. A possible mechanism for this pattern is that exotics that are more closely related to natives are more likely to share their herbivores, and thus will suffer more damage than phylogenetically isolated species. We tested this prediction using exotic plants in Ontario, Canada. We measured herbivore damage to 32 species of exotic plants in a common garden experiment, and 52 in natural populations. We estimated their phylogenetic distances from locally occurring natives in three ways: as mean distance (age) to all native plants, mean distance to native members of the same family, and distance to the closest native species. In the common garden, the proportion of leaves damaged and the average proportion of leaf area damaged declined with mean phylogenetic distance to native family relatives by late summer. Distance to native confamilials was a better predictor of damage than distance to the closest native species, while mean distance to the entire native plant community failed to predict damage. No significant patterns were detected for plants in natural populations, likely because uncontrolled site-to-site variation concealed these phylogenetic trends. To the extent that herbivory has negative demographic impacts, these results suggest that exotics that are more phylogenetically isolated from native confamilials should be more invasive; conversely, native communities should be more resistant to invasion if they harbor close familial relatives of potential invaders. However, the large scatter in this relationship suggests that these often are likely to be weak effects; as a result, these effects often may be difficult to detect in uncontrolled surveys of natural populations.

Comparative impacts of aboveground and belowground enemies on an invasive thistle.

Most research examining how herbivores and pathogens affect performance of invasive plants focuses on aboveground interactions. Although important, the role of belowground communities remains poorly understood, and the relative impact of aboveground and belowground interactions is still debated. As well, most studies of belowground interactions have been carried out in controlled environments, so little is known about the role of these interactions under natural conditions or how these relationships may change across a plant's range. Using the invasive plant Cirsium arvense, we performed a reciprocal transplant experiment to test the relative impacts of above- and belowground interactions at three sites across a 509-km latitudinal gradient in its invaded range in Ontario, Canada. At each site, C. arvense seedlings were protected with above- and/or belowground exclosures in a factorial design. Plant performance (biomass, height, stem thickness, number of leaves, length of longest leaf, maximum rhizome length) was greatest when both above- and belowground exclosures were applied and lowest when no exclosures were applied. When only one type of exclosure was applied, biomass generally improved more with belowground exclosures than with aboveground exclosures. Despite site-to-site differences in foliar damage, root damage, and mesofaunal populations, belowground interactions generally had a greater negative impact on performance than aboveground herbivory alone. These results stress the importance of including both aboveground enemy interactions and plant-soil interactions in studies of plant community dynamics and invader performance.

Sources of Controversy Surrounding Latitudinal Patterns in Herbivory and Defense.

Both herbivory and plant defenses against herbivores have been predicted to increase toward tropical regions. Early tests of this latitudinal herbivory-defense hypothesis (LHDH) were supportive, but accumulating evidence has been mixed. We argue that the lack of clarity might be due to heterogeneity in methodology and problems with study design and interpretation. We suggest possible solutions. Latitudinal studies need to carefully consider spatial and phylogenetic scale, to link plant defense measurements to herbivore performance, and to incorporate additional concepts from plant defense theory such as tolerance and induced defense. In addition, we call for consistent measures of herbivory to standardize comparisons across biomes. Improving methodology in future studies of LHDH should resolve much of the current controversy.

Revegetation following soil disturbance in a California meadow: the role of propagule supply.

Revegetation following a disturbance event initially should be constrained by the abundance and types of propagules available at the disturbed site. I tested this idea by conducting two experiments in which I created artificial soil disturbances by excavating or burying pre-existing grassland vegetation. In the first experiment, I varied disturbance intensity (depth), to investigate the consequences for revegetation when numbers of surviving propagules (dormant seeds and bulbs) were altered. In the second experiment, I varied the timing of disturbance, to investigate the consequences when disturbed sites experienced differing exposures to seasonal patterns of clonal growth and seed dispersal. I sampled these experiments from 1991 to 1993, and have interpreted their results using measurements of the seed bank, the bulb bank, and the seed rain. In the first (depth) experiment, bulbs declined in abundance with burial depth and were scarcer in deeper excavations. In contrast, numbers of annual graminoids initially showed no trends with respect to disturbance depth. These results reflect the depth distributions of the seed and bulb banks. Since bulbs occur deeply in the soil, progressively deeper disturbances left fewer survivors. Similarly, perennial graminoids could grow through the shallowest burials. In contrast, since the annual-graminoid-dominated seed bank is concentrated near the soil surface, disturbance depth mattered less to these species: any disturbance removing the surface layer was equally destructive. In the second (timing) experiment, more annual graminoids initially occurred in older plots. This result reflects seasonal patterns of seed production: plots exposed to more of the annual-graminoid-dominated seed rain supported higher densities of annual graminoids as a result. In subsequent years, the vegetation of most plots in both experiments was increasingly dominated by annual graminoids, again as a consequence of their great abundance in the seed rain. These results indicate that interactions between soil disturbances and sources of propagules play an important role in controlling early stages of succession in newly created gaps. They also suggest that disturbance may play different roles in communities characterized by species with different reproductive strategies. Understanding sources of colonists will improve our ability to predict the effects of disturbance.

Enemy release but no evolutionary loss of defence in a plant invasion: an inter-continental reciprocal transplant experiment.

When invading new regions exotic species may escape from some of their natural enemies. Reduced top-down control ("enemy release") following this escape is often invoked to explain demographic expansion of invasive species and also may alter the selective regime for invasive species: reduced damage can allow resources previously allocated to defence to be reallocated to other functions like growth and reproduction. This reallocation may provide invaders with an "evolution of increased competitive ability" over natives that defend themselves against specialist enemies. We tested for enemy release and the evolution of increased competitive ability in the North American native ragweed (Ambrosia artemisiifolia: Asteraceae), which currently is invading France. We found evidence of enemy release in natural field populations from the invaded and native ranges. Further we carried out a reciprocal transplant experiment, comparing several life history traits of plants from two North American (Ontario and South Carolina) and one French population in four common gardens on both continents. French and Canadian plants had similar flowering phenologies, flowering earlier than plants from further south in the native range. This may suggest that invasive French plants originated from similar latitudes to the Canadian population sampled. As with natural populations, experimental plants suffered far less herbivore damage in France than in Ontario. This difference in herbivory translated into increased growth but not into increased size or vigour. Moreover, we found that native genotypes were as damaged as invading ones in all experimental sites, suggesting no evolutionary loss of defence against herbivores.