Lauren P. Waller

Summary: Integrating plant physiological traits (ideal weed hypothesis) and interactions with enemies (enemy release hypothesis) may be key to understanding plant invasions. Contrary to enemy release, recent evidence suggests that invasive plants often accumulate generalist enemies due to the same r‐selected physiological traits that often drive invasive success. Despite high enemy loads, successful invasive plants can remain dominant due to high growth rates rather than due to lack of damage. Consequently, generalist herbivore and pathogen populations may be amplified by invaders and can spillover onto native plants, with these indirect interactions disproportionately affecting native rather than invasive plant species via apparent competition. Where this occurs, the generalist enemies of invasive plants may instead be hidden allies that amplify invader success and impacts.

Summary: Invasion by exotic plants is a major threat to ecosystem biodiversity globally. Although mutualistic belowground associations can play a significant role in successful invasion, studies have shown mixed results regarding the effects of plant invasion on arbuscular mycorrhizal fungi (AMF). Here, we tested how exotic dominance (i.e. invasion extent) in plant communities impacts arbuscular mycorrhizal fungal community diversity, composition, and generalism at the scale of individual plants and plant communities, and whether these impacts are explained or moderated by plant root traits (root diameter). We characterized root traits and arbuscular mycorrhizal fungal communities in the roots of native and exotic plants growing together in experimental plant communities that ranged in invasion extent (exotic plant dominance from 0% to 100%). Increases in exotic dominance decreased arbuscular mycorrhizal fungal diversity in both individual plant roots and plant communities. Greater relative abundance of generalist AMF was also observed in plant communities with increasing exotic dominance. Although root diameter affected fungal composition, it did not moderate or drive the effect of exotics. Our results highlight the role of invasion extent in understanding how arbuscular mycorrhizal fungal communities respond to exotic plant invasion and the importance of preserving belowground biodiversity.

Plant functional ecology research has primarily focused on juvenile and adult plants even though regeneration from seed can be the most consequential life‐history bottleneck with cascading influence on later stages of growth and reproduction. Understandings of relationships among phenology, morphology and growth‐related functional traits have improved our knowledge of plant life‐history strategies and adaptive responses to changing climate. However, whether relationships among phenological and morpho‐physiological traits exist during plant regeneration is unknown. We also lack understanding of the relative importance of these relationships compared with those of regeneration phenology with other factors like plant phylogeny, geographic location and whether a species is native or non‐native to the location. To better understand these gaps in knowledge, we evaluated three phenological traits (days to germination, first and third true leaves) and six morpho‐physiological traits (seed mass, relative growth rate, root elongation rate, root: shoot ratio, specific leaf area and seedling C:N) associated with regeneration for 131 forb species from six globally distributed grasslands. Morpho‐physiological traits showed several significant correlations with phenological traits. Boosted regression trees revealed that their relative importance in predicting phenological traits varied among the three phenological stages (34%–51%). Interestingly, the relative importance of morpho‐physiological traits on the phenological stages was comparable to that of phylogeny (36%–46%). In general, species with faster phenologies produced seedlings that grew faster. The influence of geographic location on phenological traits was strongest at germination (29%) and decreased (8%–15%) at later phenological stages. Native versus non‐native origin had little to no impact (0%–2%) on regeneration phenology. Strong relationships between days to germination and geographic location indicate signatures of local adaptation in the earliest life stages. Similar morpho‐physiological trait values between native and non‐native forbs imply that trait matching may be essential for non‐native establishment. While associations between phenological and morpho‐physiological traits during regeneration have not been previously recognized, our results suggest that these are complex and variable across plant regeneration. Better understanding of these associations and their variation across plant life stages may help capture species shifts with ongoing climate change and be used to develop novel approaches to seed‐based restoration. Read the free Plain Language Summary for this article on the Journal blog.

Changes in biodiversity reflect processes acting at multiple spatial scales, including globally, among habitats and within communities. This complexity makes it difficult to analyse the mechanisms that change biodiversity over time. To resolve this, we propose a novel approach to partition temporal changes in biodiversity into contributions from selection at multiple scales. We apply this approach to study changes in the biodiversity of invertebrate herbivores from a large-scale, plant community experiment. Though the experiment was designed to foster distinct insect communities due to differences in host plants, our approach shows that selection among these treatments was a negligible facet of diversity change. Instead, the dominant source of community dynamics was rapid changes in the relative abundances of individual species. These shifts produced surprisingly small changes in biodiversity. More broadly our work highlights how total change in biodiversity across a biogeographic region can be partitioned into logically distinct mechanisms.

As exotic plants invade into a new range, they can escape from specialist enemies. However, they may support generalist enemies, including both native and introduced fungal pathogens, which creates the potential for spillover and apparent competition from exotic to native plants in communities. To assess the potential for spillover of putatively pathogenic, root‐associated fungi (hereafter, ‘pathogens’) in communities invaded by exotic plants, we conducted a two‐phase plant–soil feedback experiment: a monoculture experiment with native and exotic plants grown alone and a multi‐species, community‐level experiment that ranged in the extent of exotic dominance. We used next‐generation sequencing to characterise sharing of pathogens between native and exotic plants in communities. Exotic plants outperformed natives in communities, despite harbouring higher relative abundance of generalist pathogens. The higher generalism of pathogens supported by exotic plants made them more prone to be shared with natives. The proportion of pathogens shared between exotic and native plants in communities correlated with reduced competitive ability of native compared with exotic plants. Synthesis: These data suggest that exotic plants host more generalist pathogens that are shared with native plants, which may confer an indirect benefit to exotic over native plants through apparent competition.

Changes in biodiversity reflect processes acting on the success of individual species at multiple spatial scales, including in communities, biogeographic regions, and globally. This complexity makes it difficult to analyse the mechanisms shaping diversity change using traditional approaches. To resolve this, we propose a novel approach to partition total biodiversity changes according to mechanisms reflecting species' success at multiple scales. We apply this approach to study changes in the diversity of invertebrate herbivores from a large-scale, plant community experiment. This partitioning showed that rapid changes in the relative abundances of individual species resulted in surprisingly small changes in diversity across scales. Our novel analytical method reveals how strong ecological effects at different hierarchical levels can counteract each other, resulting in weak effects on diversity across broad spatial scales.

Exotic plants can escape from specialist pathogenic microorganisms in their new range, but may simultaneously accumulate generalist pathogens. This creates the potential for pathogen spillover, which could alter plant-competitive hierarchies via apparent competition. To assess the potential for and consequences of pathogen spillover in invaded communities, we conducted a community-level plant-soil feedback experiment in experimental communities that ranged in the extent of exotic dominance, using next-generation sequencing to characterize sharing of putatively-pathogenic, root-associated fungi (hereafter, ‘pathogens’). Exotic plants outperformed natives in communities, despite being subject to stronger negative plant-soil feedbacks in monoculture and harboring higher relative abundance of pathogens. Exotic plants made more general associations with pathogens, making them more prone to sharing pathogens with natives and exerting apparent competition. These data suggest that exotic plants accumulate generalist pathogens that are shared with native plants, conferring an indirect benefit to exotic, over native plants.

Exotic plants reduce carbon sequestration: Invasive exotic plants have become a major problem worldwide, with transformational effects on the composition and function of ecosystems. In a multifactorial experiment in New Zealand, Waller et al. show that exotic plants accelerate carbon loss from soils through their interactions with invertebrate herbivores and soil biota (see the Perspective by Urcelay and Austin). They built 160 mini-ecosystems in the field, manipulating interactions among plants, invertebrate herbivores, and soil biota. Key biological and abiotic responses were measured to quantify the relative contribution and interactions of the components of each community, revealing the potential of invasive plants to influence and suppress carbon sequestration through biotic interactions. Science , this issue p. 967 ; see also p. 934

Indirect interactions mediated by shared enemies or mutualists (i.e. apparent competition) can influence whether invasive plants harm or benefit co‐occurring species. However, studies to date have largely examined single pairwise interactions, limiting our understanding of the interplay among different types of interactions and whether indirect impacts systematically favour native or exotic species. Predicting indirect interaction strength has also proven challenging, and it remains unclear whether the strengths of different indirect interactions are correlated. We conducted a field experiment in a grassland invaded by Scotch broom Cytisus scoparius to compare the strength of its indirect impacts, via both soil fungi and herbivores, on 21 native and exotic legume species growing in pots buried in the ground. Direct interactions of plants with soil fungi were controlled using nylon mesh pot windows of differing porosity (1 or 38 µm) to prevent or allow soil fungi hyphal growth. Arthropod herbivores were controlled through spraying pyrethrum pesticide. To assess indirect impacts, interactions were compared between plants adjacent to or 50 m away from an extensive Scotch broom invasion. We measured plant performance (survival, height and biomass), arthropod and hare herbivory, and rhizobia nodulation. Despite increasing arthropod herbivory of both native and exotic plant species, Scotch broom had a net positive impact on their survival and growth, through sheltering them from abiotic stress, and indirectly via beneficial soil fungi and release from hare browsing. Soil fungi also increased arthropod herbivory, decreased rhizobia nodulation and disproportionately promoted the growth of exotic plants. Overall, exotic plants experienced stronger interactions, which favoured them with beneficial soil fungi and rhizobia but not hare browsing. Finally, indirect interaction strength was not correlated among indirect interactions mediated by different interaction partners. Synthesis. We demonstrate that invaders affect their competitors through multiple interacting indirect pathways that were stronger than direct ‘nurse plant’ effects, emphasizing the importance of a community‐level approach to studying biological invasions. Exotic species experienced stronger positive and negative impacts than natives, but were facilitated overall, potentially contributing to exotic dominance in communities.