Defining invasiveness and invasibility in ecological networks

The success of a biological invasion is context dependent, and yet two key concepts—the invasiveness of species and the invasibility of recipient ecosystems—are often defined and considered separately. We propose a framework that can elucidate the complex relationship between invasibility and invasiveness. It is based on trait-mediated interactions between species and depicts the response of an ecological network to the intrusion of an alien species, drawing on the concept of community saturation. Here, invasiveness of an introduced species with a particular trait is measured by its per capita population growth rate when the initial propagule pressure of the introduced species is very low. The invasibility of the recipient habitat or ecosystem is dependent on the structure of the resident ecological network and is defined as the total width of an opportunity niche in the trait space susceptible to invasion. Invasibility is thus a measure of network instability. We also correlate invasibility with the asymptotic stability of resident ecological network, measured by the leading eigenvalue of the interaction matrix that depicts trait-based interaction intensity multiplied by encounter rate (a pairwise product of propagule pressure of all members in a community). We further examine the relationship between invasibility and network architecture, including network connectance, nestedness and modularity. We exemplify this framework with a trait-based assembly model under perturbations in ways to emulate fluctuating resources and random trait composition in ecological networks. The maximum invasiveness of a potential invader (greatest intrinsic population growth rate) was found to be positively correlated with invasibility of the recipient ecological network. Additionally, ecosystems with high network modularity and high ecological stability tend to exhibit high invasibility. Where quantitative data are lacking we propose using a qualitative interaction matrix of the ecological network perceived by a potential invader so that the structural network stability and invasibility can be estimated from the literature or from expert opinion. This approach links network structure, invasiveness and invasibility in the context of trait-mediated interactions, such as the invasion of insects into mutualistic and antagonistic networks.     

What drives invasibility? A multi‐model inference test and spatial modelling of alien plant species richness patterns in northern Portugal

Understanding and predicting biological invasions can focus either on traits that favour species invasiveness or on features of the receiving communities, habitats or landscapes that promote their invasibility. Here, we address invasibility at the regional scale, testing whether some habitats and landscapes are more invasible than others by fitting models that relate alien plant species richness to various environmental predictors. We use a multi‐model information‐theoretic approach to assess invasibility by modelling spatial and ecological patterns of alien invasion in landscape mosaics, and by testing competing hypotheses of environmental factors that may control invasibility. Because invasibility may be mediated by particular characteristics of invasiveness, we classified alien species according to their C‐S‐R plant strategies. We illustrate this approach with a set of 86 alien species in northern Portugal. We first focus on predictors influencing species richness and expressing invasibility, and then evaluate whether distinct plant strategies respond to the same or different groups of environmental predictors. We confirmed climate as a primary determinant of alien invasions, and as a primary environmental gradient determining landscape invasibility. The effects of secondary gradients were detected only when the area was sub‐sampled according to predictions based on the primary gradient. Then, multiple predictor types influenced patterns of alien species richness, with some types (landscape composition, topography and fire regime) prevailing over others. Alien species richness responded most strongly to extreme land management regimes, suggesting that intermediate disturbance induces biotic resistance by favouring native species richness. Land‐use intensification facilitated alien invasion, whereas conservation areas hosted few invaders, highlighting the importance of ecosystem stability in preventing invasions. Plants with different strategies exhibited different responses to environmental gradients, particularly when the variations of the primary gradient were narrowed by sub‐sampling. Such differential responses of plant strategies suggest using distinct control and eradication approaches for different areas and alien plant groups.     

The invasiveness of an introduced species does not predict its impact

Inconsistent use of terminology plagues the study and management of biological invasions. The term “invasive” has been used to describe inter alia (1) any introduced non-indigenous species; (2) introduced species that spread rapidly in a new region; and (3) introduced species that have harmful environmental impacts, particularly on native species. The second definition in various forms is more commonly used by ecologists, while the third definition is pervasive in policy papers and legislation. We tested the relationship between the invasiveness of an introduced species and its impact on native biodiversity. We quantified a species’ invasiveness by both its rate of establishment and its rate of spread, while its impact was assigned a categorical ranking based on the documented effects of the invader on native species populations. We found no correlations between these variables for introduced plants, mammals, fishes, invertebrates, amphibians and reptiles, suggesting that the mechanisms of invasion and impact are not strongly linked. Our results support the view that the term “invasive” should not be used to connote negative environmental impact.     

Habitat properties and plant traits interact as drivers of non‐native plant species’ seed production at the local scale

To answer the long‐standing question if we can predict plant invader success based on characteristics of the environment (invasibility) or the invasive species (invasiveness), or the combination of both, there is a need for detailed observational studies in which habitat properties, non‐native plant traits, and the resulting invader success are locally measured. In this study, we assess the interaction of gradients in the environmental and trait space on non‐native species fitness, expressed as seed production, for a set of 10 invasive and noninvasive non‐native species along a wide range of invaded sites in Flanders. In our multidimensional approach, most of the single environmental gradients (temperature, light availability, native plant species diversity, and soil fertility) and sets of non‐native plant traits (plant size, photosynthesis, and foliar chemical attributes) related positively with invader seed production. Yet correlation with seed production was much stronger when several environmental gradients were assessed in interaction, and even more so when we combined plant traits and habitat properties. The latter increased explanatory power of the models on average by 25% for invasive and by 7% for noninvasive species. Additionally, we report a 70‐fold higher seed production in invasive than in noninvasive species and fundamentally different correlations of seed production with plant traits and habitat properties in noninvasive versus invasive species. We conclude that locally measured traits and properties deserve much more attention than they currently get in invasion literature and thus encourage further studies combining this level of detail with the generality of a multiregion and multispecies approach across different stages of invasion.     

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.     

Propagule Pressure: A Null Model for Biological Invasions

Invasion ecology has been criticised for its lack of general principles. To explore this criticism, we conducted a meta-analysis that examined characteristics of invasiveness (i.e. the ability of species to establish in, spread to, or become abundant in novel communities) and invasibility (i.e. the susceptibility of habitats to the establishment or proliferation of invaders). There were few consistencies among invasiveness characteristics (3 of 13): established and abundant invaders generally occupy similar habitats as native species, while abundant species tend to be less affected by enemies; germination success and reproductive output were significantly positively associated with invasiveness when results from both stages (establishment/spread and abundance/impact) were combined. Two of six invasibility characteristics were also significant: communities experiencing more disturbance and with higher resource availability sustained greater establishment and proliferation of invaders. We also found that even though ‘propagule pressure’ was considered in only ~29% of studies, it was a significant predictor of both invasiveness and invasibility (55 of 64 total cases). Given that nonindigenous species are likely introduced non-randomly, we contend that ‘propagule biases’ may confound current paradigms in invasion ecology. Examples of patterns that could be confounded by propagule biases include characteristics of good invaders and susceptible habitats, release from enemies, evolution of ‘invasiveness’, and invasional meltdown. We conclude that propagule pressure should serve as the basis of a null model for studies of biological invasions when inferring process from patterns of invasion. An erratum to this article can be found at     

Invasiveness,invasibility and the role of environmental stress in the spread of non-native plants

Invasion ecology, the study of how organisms spread in habitats to which they are not native, asks both about the invasiveness of species and the invasibility of habitats: Which species are most likely to become invasive? Which habitats are most susceptible to invasion? To set the stage for considering these questions with regard to plants, we offer a two-way classification of nativeness and invasiveness that distinguishes natives, non-invasive non-natives and invasive non-natives. We then consider the current state of knowledge about invasiveness and invasibility. Despite much investigation, it has proven difficult to identify traits that consistently predict invasiveness. This may be largely because different traits favour invasiveness in different habitats. It has proven easier to identify types of habitats that are relatively invasible, such as islands and riverbanks. Factors thought to render habitats invasible include low intensities of competition, altered disturbance regimes and low levels of environmental stress, especially high resource availability. These factors probably often interact; the combination of altered disturbance with high resource availability may particularly promote invasibility. When biotic factors control invasibility, non-natives that are unlike native species may prove more invasive; the converse may also be true. We end with a simple conceptual model for cases in which high levels of environmental stress should and should not reduce invasibility. In some cases, it may be possible to manipulate stress to control biological invasions by plants.     

The elephant in the room: the role of failed invasions in understanding invasion biology

Most species introductions are not expected to result in invasion, and species that are invasive in one area are frequently not invasive in others. However, cases of introduced organisms that failed to invade are reported in many instances as anecdotes or are simply ignored. In this analysis, we aimed to find common characteristics between non‐invasive populations of known invasive species and evaluated how the study of failed invasions can contribute to research on biological invasions. We found intraspecific variation in invasion success and several recurring explanations for why non‐native species fail to invade; these included low propagule pressure, abiotic resistance, biotic resistance, genetic constraints and mutualist release. Furthermore, we identified key research topics where ignoring failed invasions could produce misleading results; these include studies on historical factors associated with invasions, distribution models of invasive species, the effect of species traits on invasiveness, genetic effects, biotic resistance and habitat invasibility. In conclusion, we found failed invasions can provide fundamental information on the relative importance of factors determining invasions and might be a key component of several research topics. Therefore, our analysis suggests that more specific and detailed studies on invasion failures are necessary.     

What affects the probability of biological invasions in Antarctica? Using an expanded conceptual framework to anticipate the risk of alien species expansion

Successful alien species invasion depends on many factors studied mostly in post invasion habitats, and subsequently summarized in frameworks tailored to describe the studied invasion. We used an existing expanded framework with three groups of contributing factors: habitat invisibility, system context and species invasiveness, to analyze the probability of alien species invasions in terrestrial communities of Maritime Antarctic in the future. We focused on the first two factor groups. We tested if the expanded framework could be used under a different scenario. We chose Point Thomas Oasis on King George Island to perform our analysis. Strong geographical barrier, low potential bioclimatic suitability and resource availability associated with habitat invasibility significantly reduce the likelihood of biological invasion in Antarctica. An almost full enemy release (low pressure of consumers), the high patchiness of the habitat, and the prevalence of open gaps also associated with habitat invasibility increase the possibility of invasion. The dynamics of functional connectivity, propagule pressure and spatio-temporal patterns of propagule arrival associated with human activity and climate change belonging to the system context contribute to an increase in the threat of invasions. Due to the still low land transport activity migration pathways are limited and will reduce the spread of alien terrestrial organisms by land. An effective way of preventing invasions in Antarctica seems to lie in reducing propagule pressure and eliminating alien populations as early as possible. The expanded conceptual framework opens up wider possibilities in analyzing invasions taking place in different systems and with multiple taxa.     

Giant invasive Heracleum persicum: Friend or foe of plant diversity?

The impact of invasion on diversity varies widely and remains elusive. Despite the considerable attempts to understand mechanisms of biological invasion, it is largely unknown whether some communities’ characteristics promote biological invasion, or whether some inherent characteristics of invaders enable them to invade other communities. Our aims were to assess the impact of one of the massive plant invaders of Scandinavia on vascular plant species diversity, disentangle attributes of invasible and noninvasible communities, and evaluate the relationship between invasibility and genetic diversity of a dominant invader. We studied 56 pairs of Heracleum persicum Desf. ex Fisch.‐invaded and noninvaded plots from 12 locations in northern Norway. There was lower native cover, evenness, taxonomic diversity, native biomass, and species richness in the invaded plots than in the noninvaded plots. The invaded plots had nearly two native species fewer than the noninvaded plots on average. Within the invaded plots, cover of H. persicum had a strong negative effect on the native cover, evenness, and native biomass, and a positive association with the height of the native plants. Plant communities containing only native species appeared more invasible than those that included exotic species, particularly H. persicum. Genetic diversity of H. persicum was positively correlated with invasibility but not with community diversity. The invasion of a plant community by H. persicum exerts consistent negative pressure on vascular plant diversity. The lack of positive correlation between impacts and genetic diversity of H. persicum indicates that even a small founder population may cause high impact. We highlight community stability or saturation as an important determinant of invasibility. While the invasion by H. persicum may decrease susceptibility of a plant community to further invasion, it severely reduces the abundance of native species and makes them more vulnerable to competitive exclusion.     

Resource limitation,biodiversity, and competitive effects interact to determine the invasibility of rock pool microcosms

The success of species invasions depends on both the characteristics of the invaded habitat and the traits of the invasive species. At local scales biodiversity may act as a barrier to invasion; however, the mechanism by which biodiversity confers invasion resistance to a community has been the subject of considerable debate. The purpose of this study was to test the hypothesis that productivity and diversity affected the ability of a regionally available species to colonize communities from which it is absent. We hypothesized that the invasibility of rock pool invertebrate communities would increase with increasing nutrients and decrease with increasing diversity. We tested this possibility using naturally invaded outdoor aquatic microcosms. We demonstrated that the invasibility of an experimental multi-trophic aquatic community by a competitive native midge species (Ceratopogonidae: Dasyhelea sp.) was determined by an interaction between resource availability, diversity, and the densities of two competitive ostracods species. Nutrient enrichment increased invasion success; however, within nutrient-enriched microcosms, invasion success was highest in the low-diversity treatments. Our results suggest that resource availability may in fact be the principal mechanism determining invasibility at local scales in multi-trophic rock pool communities; however resource availability can be determined by both nutrient input as well as by the diversity of the biotic community.     

Biological invasions and the neutral theory

Aim  The invasion of natural communities by alien species represents a serious threat, but creates opportunities to learn about community functions. Neutral theory proposes that the niche concept may not be needed to explain the assemblage and diversity of natural communities, challenging the classical view of community ecology and generating a lasting debate. Biological invasions, when considered as natural experiments, can be used to contrast some of the predictions of neutral and classic niche theories.
Location  Global.
Methods  We use data from biological invasions as natural experiments to contrast some of the fundamental predictions of neutral theory.
Results  Some emerging patterns did not differ from neutral model expectations (e.g. the relationship between native and exotic species richness, invasibility of resource-rich habitats, and the relationship between propagule release and invasion success). Nevertheless, other patterns (e.g. experimental evidence of the relationship between diversity and susceptibility to invasion, the invasion of communities with a low resource availability, invasiveness related to species traits) contrasted with the predictions that can be inferred from neutral theory.
Main conclusions  Neutral theory correctly highlights the need to include randomness in models of community structure. Biological invasion patterns show that neutral forces are important in structuring natural communities, but the patterns differ from those inferred from a complete neutral model. For biodiversity-conservation purposes, the implications of accepting or not accepting neutral theory as a process-based theory are very important.     

Trophic cascades in an invaded ecosystem: native keystone predators facilitate a dominant invader in an estuarine community

Determining how various factors contribute to the invasibility of systems is essential for both understanding community formation and informing management of natural areas. Research demonstrating that predators can provide biotic resistance to invasions by consuming invasive species has led to the presence of healthy predator populations being associated with reduced invasion potential of ecosystems. However, predators structure communities in many ways and their presence could also potentially facilitate invasions if they decrease populations of native species that compete with or consume an invader. We considered these two impacts of predators on invasion by analyzing the effects of two keystone predators (Pisaster spp. and Enhydra lutris nereis) on two foundation species (a native mussel Mytilus californianus and the invasive exotic bryozoan Watersipora subtorquata, a putative competitor for space with Mytilus californianus). Both native predators were found to facilitate the invasion of the exotic bryozoan, and the rate of invasion was highest when both predators were present. Facilitation of W. subtorquata occurred via indirect mechanisms that partly involved the removal of a competitor (mussels) via predation. These results illustrate that although predators can provide biotic resistance to invasion, healthy predator populations do not always confer this advantage and in fact may facilitate invasions. Therefore, implementation of management actions to enhance populations of top predators could also potentially increase the invasibility of some ecosystems.     

Propagule pressure and native species richness effects drive invasibility in tropical dry forest seedling layers

Understanding the factors that encourage or inhibit plant invasions is vital to focusing limited invasive control efforts within areas where they are most practical and cost-effective. To extend the range of contexts in which invasibility is studied and aid the development of practical strategies to limit damaging plant invasions, we set out to test the relative importance of native species richness, native seedling density, and invasive propagule pressure, on the invasibility of artificial assemblages of naturally occurring tropical woody seedling communities. Our greenhouse mesocosms included a species pool of twelve trees and woody shrubs native to South Florida's tropical hardwood hammocks, and an increasingly prevalent noxious woody invader of this system, Ardisia elliptica. We found that invader propagule pressure was the single most important factor determining community invasibility. We also revealed a positive relationship between invasibility and native species richness in our polyculture mesocosms. Because A. elliptica biomass production significantly differed among different native monocultures and was not related to overyielding in native polycultures, we suggest that the effect of species richness on invasibility in this experiment was the result of sampling effects rather than a true effect of diversity.Three broad findings hold potential for application in preventing and controlling plant invasions, especially in the seedling layers of tropical dry forests: (1) effective invasive control efforts will likely benefit from measures to minimize propagule pressure; (2) managers might do well to prioritize invasive monitoring and removal efforts on the most diverse habitats within a management region; and (3) while more data are necessary to further understand our finding of a lack of association between productivity and invasibility, management regimes aimed at maximizing primary productivity might not increase invasibility, and in fact, strategies for controlling invasive plants via the management of ecosystem productivity may be ineffective.     

Modelling invasibility in endogenously oscillating tree populations: timing of invasion matters

The timing of introduction of a new species into an ecosystem can be critical in determining the invasibility (i.e. the sensitivity to invasion) of a resident population. Here, we use an individual-based model to test how (1) the type of competition (symmetric versus asymmetric) and (2) seed masting influence the success of invasion by producing oscillatory dynamics in resident tree populations. We focus on a case where two species (one resident, one invader introduced at low density) do not differ in terms of competitive abilities. By varying the time of introduction of the invader, we show that oscillations in the resident population favour invasion, by creating “invasibility windows” during which resource is available for the invader due to transiently depressed resident population density. We discuss this result in the context of current knowledge on forest dynamics and invasions, emphasizing the importance of variability in population dynamics.     

A simulation model of plant invasion: long-distance dispersal determines the pattern of spread

Mechanisms and consequences of biological invasions are a global issue. Yet, one of the key aspects, the initial phase of invasion, is rarely observed in detail. Data from aerial photographs covering the spread of Heracleum mantegazzianum (Apiaceae, native to Caucasus) on a local scale of hectares in the Czech Republic from the beginning of invasion were used as an input for an individual-based model (IBM), based on small-scale and short-time data. To capture the population development inferred from the photographs, long-distance seed dispersal, changes in landscape structures and suitability of landscape elements to invasion by H. mantegazzianum were implemented in the model. The model was used to address (1) the role of long-distance dispersal in regional invasion dynamics, and (2) the effect of land-use changes on the progress of the invasion. Simulations showed that already small fractions of seed subjected to long-distance dispersal, as determined by systematic comparison of field data and modelling results, had an over-proportional effect on the spread of this species. The effect of land-use changes on the simulated course of invasion depends on the actual level of habitat saturation; it is larger for populations covering a high proportion of available habitat area than for those in the initial phase of invasion. Our results indicate how empirical field data and model outputs can be linked more closely with each other to improve the understanding of invasion dynamics. The multi-level, but nevertheless simple structure of our model suggests that it can be used for studying the spread of similar species invading in comparable landscapes.     

Species evenness and invasion resistance of experimental grassland communities

Concern for biodiversity loss coupled with the accelerated rate of biological invasions has provoked much interest in assessing how native plant species diversity affects invasibility. Although experimental studies extensively document the effects of species richness on invader performance, the role of species evenness in such studies is rarely examined. Species evenness warrants more attention because the relative abundances of species can account for substantially more of the variance in plant community diversity and tend to change more rapidly and more frequently in response to disturbances than the absolute numbers of species. In this study, we experimentally manipulated species evenness within native prairie grassland mesocosms. We assessed how evenness affected primary productivity, light availability and the resistance of native communities to invasion. The primary productivity of native communities increased significantly with species evenness, and this increase in productivity was accompanied by significant decreases in light availability. However, evenness had no effect on native community resistance to invasion by three common exotic invasive species. In this study, niche complementarity provides a potential mechanism for the effects of evenness on productivity and light availability, but these effects apparently were not strong enough to alter the invasibility of the experimental communities. Our results suggest that species evenness enhances community productivity but provides no benefit to invasion resistance in otherwise functionally diverse communities.     

Can Invasive Species Facilitate Native Species? Evidence of How, When, and Why These Impacts Occur

Although the predatory and competitive impacts of biological invasions are well documented, facilitation of native species by non-indigenous species is frequently overlooked. A search through recent ecological literature found that facilitative interactions between invasive and native species occur in a wide range of habitats, can have cascading effects across trophic levels, can re-structure communities, and can lead to evolutionary changes. These are critical findings that, until now, have been mostly absent from analyses of ecological impacts of biological invasions. Here I present evidence for several mechanisms that exemplify how exotic species can facilitate native species. These mechanisms include habitat modification, trophic subsidy, pollination, competitive release, and predatory release. Habitat modification is the most frequently documented mechanism, reflecting the drastic changes generated by the invasion of functionally novel habitat engineers. Further, I predict that facilitative impacts on native species will be most likely when invasive species provide a limiting resource, increase habitat complexity, functionally replace a native species, or ameliorate predation or competition. Finally, three types of facilitation (novel, substitutive, and indirect) define why exotic species can lead to facilitation of native species. It is evident that understanding biological invasions at the community and ecosystem levels will be more accurate if we integrate facilitative interactions into future ecological research. Since facilitative impacts of biological invasions can occur with native endangered species, and can have wide-ranging impacts, these results also have important implications for management, eradication, and restoration.Contribution Number 2293, Bodega Marine Laboratory, University of California at Davis.     

Amphibian richness patterns in Atlantic Forest areas invaded by American bullfrogs

The relationship between invasion success and native biodiversity is central to biological invasion research. New theoretical and analytical approaches have revealed that spatial scale, land‐use factors and community assemblages are important predictors of the relationship between community diversity and invasibility and the negative effects of invasive species on community diversity. In this study we assess if the abundance of Lithobates catesbeianus, the American bullfrog, negatively affects the richness of native amphibian species in Atlantic Forest waterbodies in Brazil. Although this species has been invading Atlantic Forest areas since the 1930s, studies that estimate the invasion effects upon native species diversity are lacking. We developed a model to understand the impact of environmental, spatial and species composition gradients on the relationships between bullfrogs and native species richness. We found a weak positive relationship between bullfrog abundance and species richness in invaded areas. The path model revealed that this is an indirect relationship mediated by community composition gradients. Our results indicate that bullfrogs are more abundant in certain amphibian communities, which can be species‐rich. Local factors describing habitat heterogeneity were the main predictors of amphibian species richness and composition and bullfrog abundance. Our results reinforce the important role of habitats in determining both native species diversity and potential invasibility.