When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses

Two venerable hypotheses, widely cited as explanations for either the success or failure of introduced species in recipient communities, are the natural enemies hypothesis and the biotic resistance hypothesis. The natural enemies hypothesis posits that introduced organisms spread rapidly because they are liberated from their co‐evolved predators, pathogens and herbivores. The biotic resistance hypothesis asserts that introduced species often fail to invade communities because strong biotic interactions with native species hinder their establishment and spread. We reviewed the evidence for both of these hypotheses as they relate to the importance of non‐domesticated herbivores in affecting the success or failure of plant invasion.
To evaluate the natural enemies hypothesis, one must determine how commonly native herbivores have population‐level impacts on native plants. If native herbivores seldom limit native plant abundance, then there is little reason to think that introduced plants benefit from escape from these enemies. Studies of native herbivore‐native plant interactions reveal that plant life‐history greatly mediates the strength with which specialist herbivores suppress plant abundance. Relatively short‐lived plants that rely on current seed production for regeneration are most vulnerable to herbivory that reduces seed production. As such, these plants may gain the greatest advantage from escaping their specialist enemies in recipient communities. In contrast, native plants that are long lived or that possess long‐lived seedbanks may not be kept “in check” by native herbivores. For these species, escape from native enemies may have little to do with their success as exotics; they are abundant both where they are native and introduced.
Evidence for native herbivores providing biotic resistance to invasion by exotics is conflicting. Our review reveals that: 1) introduced plants can attract a diverse assemblage of native herbivores and that 2) native herbivores can reduce introduced plant growth, seed set and survival. However, the generality of these impacts is unclear, and evidence that herbivory actually limits or reduces introduced plant spread is scarce. The degree to which native herbivores provide biotic resistance to either exotic plant establishment or spread may be greatly determined by their functional and numerical responses to exotic plants, which we know little about. Generalist herbivores, through their direct effects on seed dispersal and their indirect effects in altering the outcome of native–non‐native plant competitive interactions, may have more of a facilitative than negative effect on exotic plant abundance.     

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.     

It takes one to know one: Similarity to resident alien species increases establishment success of new invaders

Aim

Darwin's naturalization hypothesis states that dissimilarity to native species may benefit alien species establishment due to empty niches and reduced competition. We here add a new dimension to large‐scale tests of community invasibility, investigating the role that previously established alien species play in facilitating or hindering new invasions in plant communities.

Location

Permanent grasslands across France (including mainland and Corsica), as a receding ecosystem of great conservation importance.

Methods

Focusing on 121 alien plant species occurring in 7,215 vegetation plots, we quantified biotic similarity between new invaders and resident alien species (i.e., alien species with longer residence times) based on phylogenetic and trait distances. Additionally, we calculated distances to native species for each alien species and plot. Using multispecies distribution models, we analysed the influence of these biotic similarity measures and additional covariates on establishment success (presence/absence) of new invaders.

Results

We found that biotic similarity to resident alien species consistently increased establishment success of more recently introduced species. Phylogenetic relatedness to previous invaders had an equally strong positive effect as relatedness to native species. Conversely, trait similarity to natives hindered alien establishment as predicted by Darwin's naturalization hypothesis. These results highlight that various mechanisms may act simultaneously to determine alien establishment success.

Main conclusions

Our results suggest that, with greater similarity among alien species, invasion success increases. Such a pattern may arise either due to actual facilitation among invaders or as a result of weaker competitive interactions among invaders than between native and alien species, leading to an indirect facilitative effect. Alternatively, recent environmental changes (e.g., eutrophication, climate change) may have added new environmental filters. Determining how initial invasions might pave the road for subsequent invasions is crucial for effective multispecies management decisions and contributes a new aspect to our understanding of community assembly.

     

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.     

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.     

The impact of interactions on invasion and colonization resistance in microbial communities

In human microbiota, the prevention or promotion of invasions can be crucial to human health. Invasion outcomes, in turn, are impacted by the composition of resident communities and interactions of resident members with the invader. Here we study how interactions influence invasion outcomes in microbial communities, when interactions are primarily mediated by chemicals that are released into or consumed from the environment. We use a previously developed dynamic model which explicitly includes species abundances and the concentrations of chemicals that mediate species interaction. Using this model, we assessed how species interactions impact invasion by simulating a new species being introduced into an existing resident community. We classified invasion outcomes as resistance, augmentation, displacement, or disruption depending on whether the richness of the resident community was maintained or decreased and whether the invader was maintained in the community or went extinct. We found that as the number of invaders introduced into the resident community increased, disruption rather than augmentation became more prevalent. With more facilitation of the invader by the resident community, resistance outcomes were replaced by displacement and augmentation. By contrast, with more facilitation among residents, displacement outcomes shifted to resistance. When facilitation of the resident community by the invader was eliminated, the majority of augmentation outcomes turned into displacement, while when inhibition of residents by invaders was eliminated, invasion outcomes were largely unaffected. Our results suggest that a better understanding of interactions within resident communities and between residents and invaders is crucial to predicting the success of invasions into microbial communities.     

The importance of biological inertia in plant community resistance to invasion

Abstract. Insights into the ecology of historic invasions by introduced species can be gained by studying long‐term patterns of invasions by native species. In this paper, we review literature in palaeo‐ecology, forest‐stand simulation modelling, and historical studies of plant species invasions to illustrate the relevance of biological inertia in plant communities to invasion ecology. Resistance to invasion occurs in part because of environmental, demographic, and biotic factors influencing the arrival and establishment of invading species. We propose that biological inertia within the resident community is a fourth component of resistance to invasion, because of the lag time inherent in eliminating resident species and perhaps their traces after environmental conditions become suitable for invasion by immigrating species. Whether or not an introduced species invades can be conditioned by the presence of the pre‐existing community (and/or its legacy) in addition to the other biotic and abiotic factors.     

When does ecosystem engineering cause invasion and species replacement?

Introduced exotic species can dominate communities and replace native species that should be better adapted to their local environment, a paradox that is usually explained by the absence of natural enemies and by habitat alteration resulting from anthropogenic disturbance. Additionally, introduced species can enhance their invasion success and impact on native species by modifying selection pressures in their new environment through ecosystem engineering. We analyse a simple dynamic model of indirect competition for habitat between a non-engineering resident species and an engineering exotic species. The conditions for invasion and competitive exclusion of the resident by the exotic species and the range of dynamic outcomes suggested by the model are determined by the form of density dependence. We give simple criteria for the success of the invading species on dimensionless quantities involving rates of ecosystem engineering and of habitat degradation. The model's predictions offer an additional explanation for a range of invasion dynamics reported in the literature, including lag times between introduction and establishment. One intriguing result is that a series of failed invasions may successively reduce environmental resistance to subsequent invasion, through a cumulative effect of habitat transformation. More work is needed to determine the frequency and conditions in which engineering is required for successful establishment, and whether highly-successful (or high-impact) invaders are more likely to possess ecosystem engineering traits.     

Differential invasion success of salmonids in southern Chile: patterns and hypotheses

Biological invasions create complex ecological and societal issues worldwide. Most of the knowledge about invasions comes only from successful invaders, but less is known about which processes determine the differential success of invasions. In this review, we develop a framework to identify the main dimensions driving the success and failure of invaders, including human influences, characteristics of the invader, and biotic interactions. We apply this framework by contrasting hypotheses and available evidence to explain variability in invasion success for 12 salmonids introduced to Chile. The success of Oncorhynchus mykiss and Salmo trutta seems to be influenced by a context-specific combination of their phenotypic plasticity, low ecosystem resistance, and propagule pressure. These well-established invaders may limit the success of subsequently introduced salmonids, with the possible exception of O. tshawytscha, which has a short freshwater residency and limited spatial overlap with trout. Although propagule pressure is high for O. kisutch and S. salar due to their intensive use in aquaculture, their lack of success in Chile may be explained by environmental resistance, including earlier spawning times than in their native ranges, and interactions with previously established and resident Rainbow Trout. Other salmonids have also failed to establish, and they exhibit a suite of ecological traits, environmental resistance, and limited propagule pressure that are variably associated with their lack of success. Collectively, understanding how the various drivers of invasion success interact may explain the differential success of invaders and provide key guidance for managing both positive and negative outcomes associated with their presence.     

Biotic resistance buffers the effects of nutrient enrichment on the success of a highly invasive aquatic plant

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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.     

Global ecological impacts of invasive species in aquatic ecosystems

The introduction of invasive species, which often differ functionally from the components of the recipient community, generates ecological impacts that propagate along the food web. This review aims to determine how consistent the impacts of aquatic invasions are across taxa and habitats. To that end, we present a global meta‐analysis from 151 publications (733 cases), covering a wide range of invaders (primary producers, filter collectors, omnivores and predators), resident aquatic community components (macrophytes, phytoplankton, zooplankton, benthic invertebrates and fish) and habitats (rivers, lakes and estuaries). Our synthesis suggests a strong negative influence of invasive species on the abundance of aquatic communities, particularly macrophytes, zooplankton and fish. In contrast, there was no general evidence for a decrease in species diversity in invaded habitats, suggesting a time lag between rapid abundance changes and local extinctions. Invaded habitats showed increased water turbidity, nitrogen and organic matter concentration, which are related to the capacity of invaders to transform habitats and increase eutrophication. The expansion of invasive macrophytes caused the largest decrease in fish abundance, the filtering activity of filter collectors depleted planktonic communities, omnivores (including both facultative and obligate herbivores) were responsible for the greatest decline in macrophyte abundance, and benthic invertebrates were most negatively affected by the introduction of new predators. These impacts were relatively consistent across habitats and experimental approaches. Based on our results, we propose a framework of positive and negative links between invasive species at four trophic positions and the five different components of recipient communities. This framework incorporates both direct biotic interactions (predation, competition, grazing) and indirect changes to the water physicochemical conditions mediated by invaders (habitat alteration). Considering the strong trophic links that characterize aquatic ecosystems, this framework is relevant to anticipate the far‐reaching consequences of biological invasions on the structure and functionality of aquatic ecosystems.     

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.     

Global synthesis suggests that food web connectance correlates to invasion resistance

Biological invasions are a key component of global change, and understanding the drivers of global invasion patterns will aid in assessing and mitigating the impact of invasive species. While invasive species are most often studied in the context of one or two trophic levels, in reality species invade communities comprised of complex food webs. The complexity and integrity of the native food web may be a more important determinant of invasion success than the strength of interactions between a small subset of species within a larger food web. Previous efforts to understand the relationship between food web properties and species invasions have been primarily theoretical and have yielded mixed results. Here, we present a synthesis of empirical information on food web connectance and species invasion success gathered from different sources (estimates of food web connectance from the primary literature and estimates of invasion success from the Global Invasive Species Database as well as the primary literature). Our results suggest that higher‐connectance food webs tend to host fewer invaders and exert stronger biotic resistance compared to low‐connectance webs. We argue that while these correlations cannot be used to infer a causal link between food web connectance and habitat invasibility, the promising findings beg for further empirical research that deliberately tests for relationships between food web connectance and invasion.     

Invasive plants may promote predator‐mediated feedback that inhibits further invasion

Understanding the impacts of invasive species requires placing invasion within a full community context. Plant invaders are often considered in the context of herbivores that may drive invasion by avoiding invaders while consuming natives (enemy escape), or inhibit invasion by consuming invaders (biotic resistance). However, predators that attack those herbivores are rarely considered as major players in invasion. Invasive plants often promote predators, generally by providing improved habitat. Here, we show that predator‐promoting invaders may initiate a negative feedback loop that inhibits invasion. By enabling top‐down control of herbivores, predator‐promoting invaders lose any advantage gained through enemy escape, indirectly favoring natives. In cases where palatable invaders encounter biotic resistance, predator promotion may allow an invader to persist, but not dominate. Overall, results indicate that placing invaders in a full community context may reveal reduced impacts of invaders compared to expectations based on simple plant–plant or plant–herbivore subsystems.     

Ecology of forest insect invasions

Forests in virtually all regions of the world are being affected by invasions of non-native insects. We conducted an in-depth review of the traits of successful invasive forest insects and the ecological processes involved in insect invasions across the universal invasion phases (transport and arrival, establishment, spread and impacts). Most forest insect invasions are accidental consequences of international trade. The dominant invasion ‘pathways’ are live plant imports, shipment of solid wood packaging material, “hitchhiking” on inanimate objects, and intentional introductions of biological control agents. Invading insects exhibit a variety of life histories and include herbivores, detritivores, predators and parasitoids. Herbivores are considered the most damaging and include wood-borers, sap-feeders, foliage-feeders and seed eaters. Most non-native herbivorous forest insects apparently cause little noticeable damage but some species have profoundly altered the composition and ecological functioning of forests. In some cases, non-native herbivorous insects have virtually eliminated their hosts, resulting in major changes in forest composition and ecosystem processes. Invasive predators (e.g., wasps and ants) can have major effects on forest communities. Some parasitoids have caused the decline of native hosts. Key ecological factors during the successive invasion phases are illustrated. Escape from natural enemies explains some of the extreme impacts of forest herbivores but in other cases, severe impacts result from a lack of host defenses due to a lack of evolutionary exposure. Many aspects of forest insect invasions remain poorly understood including indirect impacts via apparent competition and facilitation of other invaders, which are often cryptic and not well studied.     

Strong invaders are strong defenders – implications for the resistance of invaded communities

Many ecosystems receive a steady stream of non‐native species. How biotic resistance develops over time in these ecosystems will depend on how established invaders contribute to subsequent resistance. If invasion success and defence capacity (i.e. contribution to resistance) are correlated, then community resistance should increase as species accumulate. If successful invaders also cause most impact (through replacing native species with low defence capacity) then the effect will be even stronger. If successful invaders instead have weak defence capacity or even facilitative attributes, then resistance should decrease with time, as proposed by the invasional meltdown hypothesis. We analysed 1157 introductions of freshwater fish in Swedish lakes and found that species’ invasion success was positively correlated with their defence capacity and impact, suggesting that these communities will develop stronger resistance over time. These insights can be used to identify scenarios where invading species are expected to cause large impact.     

Extended leaf phenology may drive plant invasion through direct and apparent competition

Invasive plants can inflict great harm, yet drivers of successful invasion remain unclear. Many invaders of North American deciduous forests exhibit extended leaf phenology (ELP), or longer growing season relative to natives. ELP may grant invaders competitive advantages, but we argue that ELP more potently drives invasion in the presence of herbivores. ELP invaders can support herbivores by lessening starvation during winter; consequently, native plants may suffer when attacked later through apparent competition. As modeled here, even short ELP can promote competitive success of invaders, and apparent competition sharply enhances ELP invader dominance. In ‘partial enemy escape’ scenarios, a less palatable ELP invader nearly excludes a preferred native where an invader without ELP could not. Together, ELP and apparent competition enhance invasion even when biotic resistance should suppress it, i.e. when the invader competes weakly or provides preferred forage. Thus, ELP‐apparent competition interactions grant invaders considerable success while challenging core tenets of invasion ecology.     

Abiotic conditions shape the relationship between indigenous and exotic species richness in a montane biodiversity hotspot

Montane ecosystems are more prone to invasions by exotic plant species than previously thought. Besides abiotic factors, such as climate and soil properties, plant-plant interactions within communities are likely to affect the performance of potential invaders in their exotic range. The biotic resistance hypothesis predicts that high indigenous species richness hampers plant invasions. The biotic acceptance hypothesis, on the other hand, predicts a positive relationship between indigenous and exotic species richness. We tested these two hypotheses using observational data along an elevational gradient in a southern African biodiversity hotspot. Species composition data of indigenous and exotic plants were recorded in 20 road verge plots along a gradient of 1775–2775 m a.s.l. in the Drakensberg, South Africa. Plots were 2?×?50 m in size and positioned at 50 m elevational intervals. We found a negative correlation between indigenous and exotic richness for locations with poorly developed mineral soils, suggesting biotic resistance through competitive interactions. A strong positive correlation for plots with very shallow soils at high elevations indicated a lack of biotic resistance and the possibility of facilitating interactions in harsher environments. These results suggest that biotic resistance is restricted to the lower and mid elevations while biotic acceptance prevails in presence of severe abiotic stress, potentially increasing the risk of plant invasions into montane biodiversity hotspots.