Traits linked with species invasiveness and community invasibility vary with time,stage and indicator of invasion in a long‐term grassland experiment

Much uncertainty remains about traits linked with successful invasion – the establishment and spread of non‐resident species into existing communities. Using a 20‐year experiment, where 50 non‐resident (but mostly native) grassland plant species were sown into savannah plots, we ask how traits linked with invasion depend on invasion stage (establishment, spread), indicator of invasion success (occupancy, relative abundance), time, environmental conditions, propagule rain, and traits of invaders and invaded communities. Trait data for 164 taxa showed that invader occupancy was primarily associated with traits of invaders, traits of recipient communities, and invader‐community interactions. Invader abundance was more strongly associated with community traits (e.g. proportion legume) and trait differences between invaders and the most similar resident species. Annuals and invaders with high‐specific leaf area were only successful early in stand development, whereas invaders with conservative carbon capture strategies persisted long‐term. Our results indicate that invasion is context‐dependent and long‐term experiments are required to comprehensively understand invasions.     

Facilitation promotes invasions in plant‐associated microbial communities

While several studies have established a positive correlation between community diversity and invasion resistance, it is less clear how species interactions within resident communities shape this process. Here, we experimentally tested how antagonistic and facilitative pairwise interactions within resident model microbial communities predict invasion by the plant–pathogenic bacterium Ralstonia solanacearum. We found that facilitative resident community interactions promoted and antagonistic interactions suppressed invasions both in the lab and in the tomato plant rhizosphere. Crucially, pairwise interactions reliably explained observed invasion outcomes also in multispecies communities, and mechanistically, this was linked to direct inhibition of the invader by antagonistic communities (antibiosis), and to a lesser degree by resource competition between members of the resident community and the invader. Together, our findings suggest that the type and strength of pairwise interactions can reliably predict the outcome of invasions in more complex multispecies communities.     

A meta-analysis of biotic resistance to exotic plant invasions

Biotic resistance describes the ability of resident species in a community to reduce the success of exotic invasions. Although resistance is a well‐accepted phenomenon, less clear are the processes that contribute most to it, and whether those processes are strong enough to completely repel invaders. Current perceptions of strong, competition‐driven biotic resistance stem from classic ecological theory, Elton's formulation of ecological resistance, and the general acceptance of the enemies‐release hypothesis. We conducted a meta‐analysis of the plant invasions literature to quantify the contribution of resident competitors, diversity, herbivores and soil fungal communities to biotic resistance. Results indicated large negative effects of all factors except fungal communities on invader establishment and performance. Contrary to predictions derived from the natural enemies hypothesis, resident herbivores reduced invasion success as effectively as resident competitors. Although biotic resistance significantly reduced the establishment of individual invaders, we found little evidence that species interactions completely repelled invasions. We conclude that ecological interactions rarely enable communities to resist invasion, but instead constrain the abundance of invasive species once they have successfully established.     

Elevated success of multispecies bacterial invasions impacts community composition during ecological succession

Successful microbial invasions are determined by a species’ ability to occupy a niche in the new habitat whilst resisting competitive exclusion by the resident community. Despite the recognised importance of biotic factors in determining the invasiveness of microbial communities, the success and impact of multiple concurrent invaders on the resident community has not been examined. Simultaneous invasions might have synergistic effects, for example if resident species need to exhibit divergent phenotypes to compete with the invasive populations. We used three phylogenetically diverse bacterial species to invade two compositionally distinct communities in a controlled, naturalised in vitro system. By initiating the invader introductions at different stages of succession, we could disentangle the relative importance of resident community structure, invader diversity and time pre‐invasion. Our results indicate that multiple invaders increase overall invasion success, but do not alter the successional trajectory of the whole community.     

Abiotic and biotic resistance to grass invasion in serpentine annual plant communities

Biological invasions severely impact native plant communities, causing dramatic shifts in species composition and the restriction of native species to spatially isolated refuges. Competition from resident species and the interaction between resource limitation and competition have been overlooked as mechanisms of community resistance in refugia habitats. We examined the importance of these factors in determining the resistance of California serpentine plant communities to invasion by three common European grasses, Avena barbata, Bromus diandrus, and Hordeum murinum. We added seeds of each of these grasses to plots subjected to six levels of resource addition (N, P, Ca, H₂O, all resources together, and a no-addition control) and two levels of competition (with resident community present or removed). Resource limitation and competition had strong effects on the biomass and reproduction of the three invaders. The addition of all resources together combined with the removal of the resident community yielded individual plants that were fourfold to 20-fold larger and sixfold to 20-fold more fecund than plants from control plots. Competitor removal alone yielded invaders that were twofold to sevenfold larger and twofold to ninefold more fecund. N addition alone or in combination with other resources led to a twofold to ninefold increase in the biomass and fecundity of the invaders. No other resource alone significantly affected native or invader performance, suggesting that N was the key limiting resource during our experiment. We found a significant interaction between abiotic and biotic resistance for Bromus, which experienced increased competitive suppression in fertilized plots. The threefold increase in resident biomass with N addition was likely responsible for this result. Our results confirm that serpentine plant communities are severely N limited, which, in combination with competition from resident species, promotes the resistance of these systems to invasions. Our work suggests that better understanding the relative sensitivities of invaders and residents to the physical environment is critical to predicting how abiotic and biotic factors interact to determine community resistance.     

Siderophores drive invasion dynamics in bacterial communities through their dual role as public good versus public bad

Microbial invasions can compromise ecosystem services and spur dysbiosis and disease in hosts. Nevertheless, the mechanisms determining invasion outcomes often remain unclear. Here, we examine the role of iron-scavenging siderophores in driving invasions of Pseudomonas aeruginosa into resident communities of environmental pseudomonads. Siderophores can be ‘public goods’ by delivering iron to individuals possessing matching receptors; but they can also be ‘public bads’ by withholding iron from competitors lacking these receptors. Accordingly, siderophores should either promote or impede invasion, depending on their effects on invader and resident growth. Using supernatant feeding and invasion assays, we show that invasion success indeed increased when the invader could use its siderophores to inhibit (public bad) rather than stimulate (public good) resident growth. Conversely, invasion success decreased the more the invader was inhibited by the residents’ siderophores. Our findings identify siderophores as a major driver of invasion dynamics in bacterial communities under iron-limited conditions.     

Phenotypic plasticity opposes species invasions by altering fitness surface

Understanding species invasion is a central problem in ecology because invasions of exotic species severely impact ecosystems, and because invasions underlie fundamental ecological processes. However, the influence on invasions of phenotypic plasticity, a key component of many species interactions, is unknown. We present a model in which phenotypic plasticity of a resident species increases its ability to oppose invaders, and plasticity of an invader increases its ability to displace residents. Whereas these effects are expected due to increased fitness associated with phenotypic plasticity, the model additionally reveals a new and unforeseen mechanism by which plasticity affects invasions: phenotypic plasticity increases the steepness of the fitness surface, thereby making invasion more difficult, even by phenotypically plastic invaders. Our results should apply to phenotypically plastic responses to any fluctuating environmental factors including predation risk, and to other factors that affect the fitness surface such as the generalism of predators. We extend the results to competition, and argue that phenotypic plasticity's effect on the fitness surface will destabilize coexistence at local scales, but stabilize coexistence at regional scales. Our study emphasizes the need to incorporate variable interaction strengths due to phenotypic plasticity into invasion biology and ecological theory on competition and coexistence in fragmented landscapes.     

Species diversity reduces invasion success in pathogen‐regulated communities

The loss of natural enemies is thought to explain why certain invasive species are so spectacularly successful in their introduced range. However, if losing natural enemies leads to unregulated population growth, this implies that native species are themselves normally subject to natural enemy regulation. One possible widespread mechanism of natural enemy regulation is negative soil feedbacks, in which resident species growing on home soils are disadvantaged because of a build‐up of species‐specific soil pathogens. Here we construct simple models in which pathogens cause resident species to suffer reduced competitive ability on home soils and consider the consequences of such pathogen regulation for potential invading species. We show that the probability of successful invasion and its timescale depend strongly on the competitive ability of the invader on resident soils, but are unaffected by whether or not the invader also suffers reduced competitive ability on home soils (i.e. pathogen regulation). This is because, at the start of an invasion, the invader is rare and hence mostly encounters resident soils. However, the lack of pathogen regulation does allow the invader to achieve an unusually high population density. We also show that increasing resident species diversity in a pathogen‐regulated community increases invasion resistance by reducing the frequency of home‐site encounters. Diverse communities are more resistant to invasion than monocultures of the component species: they preclude a greater range of potential invaders, slow the timescale of invasion and reduce invader population size. Thus, widespread pathogen regulation of resident species is a potential explanation for the empirical observation that diverse communities are more invasion resistant.     

Evolutionary game theory as a framework for studying biological invasions

Although biological invasions pose serious threats to biodiversity, they also provide the opportunity to better understand interactions between the ecological and evolutionary processes structuring populations and communities. However, ecoevolutionary frameworks for studying species invasions are lacking. We propose using game theory and the concept of an evolutionarily stable strategy (ESS) as a conceptual framework for integrating the ecological and evolutionary dynamics of invasions. We suggest that the pathways by which a recipient community may have no ESS provide mechanistic hypotheses for how such communities may be vulnerable to invasion and how invaders can exploit these vulnerabilities. We distinguish among these pathways by formalizing the evolutionary contexts of the invader relative to the recipient community. We model both the ecological and the adaptive dynamics of the interacting species. We show how the ESS concept provides new mechanistic hypotheses for when invasions result in long- or short-term increases in biodiversity, species replacement, and subsequent evolutionary changes.     

Is biotic resistance enhanced by natural variation in diversity?

Theories linking diversity to ecosystem function have been challenged by the widespread observation of more exotic species in more diverse native communities. Few studies have addressed the underlying processes by dissecting how biotic resistance to new invaders may be shaped by the same environmental influences that determine diversity and other community properties. In grasslands with heterogeneous soils, we added invaders and removed competitors to analyze the causes of invasion resistance. Abiotic resistance was measured using invader success in the absence of the resident community. Biotic resistance was measured as the reduction in invader success in the presence of the resident community. Invaders were most successful where biotic resistance was lowest and abiotic resistance was highest, confirming the dominant role of biotic resistance. Contrary to theory, though, biotic resistance was highest where both species richness and functional diversity were lowest. In the multivariate framework of a structural equation model, biotic resistance was independent of community diversity, and was highest where fertile soils led to high community biomass. Seed predation slightly augmented biotic resistance without qualitatively changing the results. Soil‐related genotypic variation in the invader also did not affect the results. We conclude that in natural systems, diversity may be correlated with invasibility and yet have little effect on biotic resistance to invasion. More generally, the environmental causes of variation in diversity should be considered when examining the potential functional consequences of diversity.     

Can limiting similarity increase invasion resistance? A meta‐analysis of experimental studies

Synthesis We used meta‐analyses to examine experimental evidence that functional similarity between invaders and resident communities reduces invasion. We synthesized evidence from studies that experimentally added seed to resident communities in which the functional group composition had been manipulated. We found communities containing functionally similar resident species reduced invasion of forb but not grass invaders. However, experimental design dramatically influenced the results – with evidence for limiting similarity only found in artificially assembled communities, and not when studies used functional group removal from more ‘natural communities’. We suggest that functional group similarity plays a limited role in biotic resistance in established communities. The principle of limiting similarity suggests that species must be functionally different to coexist; based on the assumption that inter‐specific competition should be greatest between functionally similar species. There has been controversy over the generality of this assembly rule for plant communities with some studies finding evidence for limiting similarity and others not. One approach to testing this is to examine the ‘invasion’ success of species into communities in which the functional group composition has been manipulated. Using a meta‐analysis approach, we examined the generality of limiting similarity for plant communities based on published experimental studies. We asked – is establishment of an invading species less successful if it belongs to a functional group that is already present in the community compared to a community in which that functional group is absent? We explored separately colonisation (i.e. germination, establishment or seedling survival) and performance (i.e. biomass, cover or growth) of different functional groups (forbs and grasses) and experimental designs (removal experiments of more or less natural communities and synthetic‐assemblage experiments). We found that communities containing functionally similar resident species did reduce invader colonisation and performance of forb invaders, but did not reduce colonisation or performance of grass invaders. Evidence in support of limiting similarity was only detected in synthetic‐assemblage experiments and not when studies used functional group removal from ‘natural’ communities. Functional similarity is an important aspect of biotic resistance for forb invaders, but was only found in artificial communities. This has implications for restoration ecology especially when communities are built de novo. However, we suggest that limiting similarity plays a limited role in biotic resistance, because no evidence was detected in established communities.     

Productivity, herbivory, and species traits rather than diversity influence invasibility of experimental phytoplankton communities

Biological invasions are a major threat to natural biodiversity; hence, understanding the mechanisms underlying invasibility (i.e., the susceptibility of a community to invasions by new species) is crucial. Invasibility of a resident community may be affected by a complex but hitherto hardly understood interplay of (1) productivity of the habitat, (2) diversity, (3) herbivory, and (4) the characteristics of both invasive and resident species. Using experimental phytoplankton microcosms, we investigated the effect of nutrient supply and species diversity on the invasibility of resident communities for two functionally different invaders in the presence or absence of an herbivore. With increasing nutrient supply, increased herbivore abundance indicated enhanced phytoplankton biomass production, and the invasion success of both invaders showed a unimodal pattern. At low nutrient supply (i.e., low influence of herbivory), the invasibility depended mainly on the competitive abilities of the invaders, whereas at high nutrient supply, the susceptibility to herbivory dominated. This resulted in different optimum nutrient levels for invasion success of the two species due to their individual functional traits. To test the effect of diversity on invasibility, a species richness gradient was generated by random selection from a resident species pool at an intermediate nutrient level. Invasibility was not affected by species richness; instead, it was driven by the functional traits of the resident and/or invasive species mediated by herbivore density. Overall, herbivory was the driving factor for invasibility of phytoplankton communities, which implies that other factors affecting the intensity of herbivory (e.g., productivity or edibility of primary producers) indirectly influence invasions.     

Does disturbance,competition or resource limitation underlie Hieracium lepidulum invasion in New Zealand? Mechanisms of establishment and persistence,and functional differentiation among invasive and native species

The processes underlying plant invasions have been the subject of much ecological research. Understanding mechanisms of plant invasions are difficult to elucidate from observations, yet are crucial for ecological management of invasions. Hieracium lepidulum, an asteraceous invader in New Zealand, is a species for which several explanatory mechanisms can be raised. Alternative mechanisms, including competitive dominance, disturbance of resident vegetation allowing competitive release or nutrient resource limitation reducing competition with the invader are raised to explain invasion. We tested these hypotheses in two field experiments which manipulated competitive, disturbance and nutrient environments in pre‐invasion and post‐invasion vegetation. H. lepidulum and resident responses to environmental treatments were measured to allow interpretation of underlying mechanisms of establishment and persistence. We found that H. lepidulum differed in functional response profile from native species. We also found that other exotic invaders at the sites were functionally different to H. lepidulum in their responses. These data support the hypothesis that different invaders use different invasion mechanisms from one another. These data also suggest that functional differentiation between invaders and native resident vegetation may be an important contributing factor allowing invasion. H. lepidulum appeared to have little direct competitive effect on post‐invasion vegetation, suggesting that competition was not a dominant mechanism maintaining its persistence. There was weak support for disturbance allowing initial establishment of H. lepidulum in pre‐invasion vegetation, but disturbance did not lead to invader dominance. Strong support for nutrient limitation of resident species was provided by the rapid competitive responses with added nutrients despite presence of H. lepidulum. Rapid competitive suppression of H. lepidulum once nutrient limitation was alleviated suggests that nutrient limitation may be an important process allowing the invader to dominate. Possible roles of historical site degradation and/or invader‐induced soil chemical/microbial changes in nutrient availability are discussed.     

Distinct invasion strategies operating within a natural annual plant system

Alien plant species are known to have a wide range of impacts on recipient communities, from resident species’ exclusions to coexistence with resident species. It remains unclear; however, if this variety of impacts is due to different invader strategies, features of recipient communities or both. To test this, we examined multiple plant invasions of a single ecosystem in southwestern Australia. We used extensive community data to calculate pairwise segregation between target alien species and many co‐occurring species. We related segregation to species’ positions along community trait hierarchies and identified at least two distinct invasion strategies: ‘exploiters’ which occupy high positions along key trait hierarchies and reduce local native species diversity (particularly in nutrient‐enriched situations), and ‘coexisters’ who occupy intermediate trait positions and have no discernable impact on native diversity. We conclude that trait hierarchies, linked to measures of competition, can provide valuable insights about the processes driving different invasion outcomes.     

Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities?

Biological invasions dramatically affect the distribution, abundance and reproduction of many native species. Because of these ecological effects, exotic species can also influence the evolution of natives exposed to novel interactions with invaders. Evolutionary changes in natives in response to selection from exotics are usually overlooked, yet common responses include altered anti-predator defenses, changes in the spectrum of resources and habitats used, and other adaptations that allow native populations to persist in invaded areas. Whether a native population is capable of responding evolutionarily to selection from invaders will depend on the demographic impact of the invader, the genetic architecture and genetic variability of the native population and potentially the history of previous invasions. In some cases, natives will fail to evolve or otherwise adapt, and local or global extinction will result. In other cases, adaptive change in natives may diminish impacts of invaders and potentially promote coexistence between invaders and natives. Here, we review the evidence for evolutionary responses of native species to novel community members. We also discuss how the effects of introduced species may differ from those caused by natural range expansions of native species. Notably, introduced species may come from remote biotas with no previous evolutionary history with the native community. In addition, the rate of addition of introduced species into communities is much greater than all but the most extreme cases of historical biotic exchange. Understanding the evolutionary component of exotic/native species interactions is critical to recognizing the long-term impacts of biological invasions, and to understanding the role of evolutionary processes in the assembly and dynamics of natural communities.     

Extended leaf phenology in deciduous forest invaders: mechanisms of impact on native communities

Many high‐impact invaders of temperate deciduous forests of Eastern North America exhibit extended leaf phenology compared to native species, with leaf emergence occurring earlier in the spring and abscission occurring later in the autumn. This observation indicates that extended phenology may be an important invasion mechanism for this system. However, most evidence that extended leaf phenology drives species invasion is anecdotal, and most studies that directly address the role of leaf phenology in invasion focus solely on increased invader growth. Beyond increasing invader growth, extended leaf phenology may drive invader impact on natives by (1) facilitating resource competition through nutrient pre‐emption and shading, (2) altering production of secondary chemicals by invasive plants, (3) altering apparent competition dynamics mediated by native herbivores, (4) allowing temporal enemy escape, and (5) altering behaviour of native pollinators. I review current evidence from the literature regarding each of these possible consequences of extended invader phenology and emphasize the need for experimental manipulations to measure the extent to which extended leaf phenology mediates impact on the native community. Understanding the importance of leaf phenology in species invasion will facilitate prevention of future invasions while elucidating the role of seasonality in shaping species interactions.     

Invasions cause biodiversity loss and community simplification in vertebrate food webs

Global change is increasing the occurrence of perturbation events on natural communities, with biological invasions posing a major threat to ecosystem integrity and functioning worldwide. Most studies addressing biological invasions have focused on individual species or taxonomic groups to understand both, the factors determining invasion success and their effects on native species. A more holistic approach that considers multispecies communities and species’ interactions can contribute to a better understanding of invasion effects on complex communities. Here we address biological invasions on species‐rich food webs. We performed in silico experiments on empirical vertebrate food webs by introducing virtual species characterised by different ecological roles and belonging to different trophic groups. We varied a number of invasive species traits, including their diet breadth, the number of predators attacking them, and the bioenergetic thresholds below which invader and native species become extinct. We found that simpler food webs were more vulnerable to invasions, and that relatively less connected mammals were the most successful invaders. Invasions altered food web structure by decreasing species richness and the number of links per species, with most extinctions affecting poorly connected birds. Our food web approach allows identifying the combinations of trophic factors that facilitate or prevent biological invasions, and it provides testable predictions on the effects of invasions on the structure and dynamics of multitrophic communities.     

Every Coin Has a Back Side: Invasion by Limnohabitans planktonicus Promotes the Maintenance of Species Diversity in Bacterial Communities

One of the earliest challenges for ecologists has been to study the impact of invasive species on microbial communities. Although bacteria are fundamental in biological processes, current knowledge on invasion effects by aquatic non-pathogenic bacteria is still limited. Using pure cultures of diverse planktonic bacteria as model organisms at two different carbon concentration levels, we tested the response of an assembled community to the invasion by Limnohabitans planktonicus, an opportunistic bacterium, successful in freshwaters. The invader, introduced at the early stationary growth phase of the resident community, caused a strong decrement of the abundance of the dominant species. This was due to competition for nutrients and a potential allelopathic interaction. Simultaneously, resident species formerly unable to successfully compete within the community, thus potentially exposed to competitive exclusion, increased their abundances. The overall result of the invasion was preservation of species diversity, the higher the lower was the substrate content available. Our study provides new insights into bacterial invasions, offering an alternative interpretation of invasions for community ecology.     

Roles of parasites in animal invasions

Biological invasions are global threats to biodiversity and parasites might play a role in determining invasion outcomes. Transmission of parasites from invading to native species can occur, aiding the invasion process, whilst the 'release' of invaders from parasites can also facilitate invasions. Parasites might also have indirect effects on the outcomes of invasions by mediating a range of competitive and predatory interactions among native and invading species. Although pathogen outbreaks can cause catastrophic species loss with knock-on effects for community structure, it is less clear what impact persistent, sub-lethal parasitism has on native-invader interactions and community structure. Here, we show that the influence of parasitism on the outcomes of animal invasions is more subtle and wide ranging than has been previously realized.