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.     

Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids?

Biological invasions are ecologically and economically costly. Understanding the major mechanisms that contribute to an alien species becoming invasive is seen as essential for limiting the effects of invasive alien species. However, there are a number of fundamental questions that need addressing such as why some communities are more vulnerable to invasion than others and, indeed, why some alien species become widespread and abundant. The enemy release hypothesis (ERH) is widely evoked to explain the establishment and proliferation of an alien species. ERH predicts that an alien species introduced to a new region should experience a decrease in regulation by natural enemies which will lead to an increase in the distribution and abundance of the alien species. At the centre of this theory is the assumption that natural enemies are important regulators of populations. Additionally, the theory implies that such natural enemies have a stronger regulatory effect on native species than they do on alien species in the introduced range, and this disparity in enemy regulation results in increased population growth of the alien species. However, empirical evidence for the role of the ERH in invasion success is lacking, particularly for invertebrates. Many studies equate a reduction in the number of natural enemies associated with an alien species to release without studying population effects. Further insight is required in relation to the effects of specific natural enemies on alien and native species (particularly their ability to regulate populations). We review the role of ecological models in exploring ERH. We suggest that recent developments in molecular technologies offer considerable promise for investigating ERH in a community context.     

Release from belowground enemies and shifts in root traits as interrelated drivers of alien plant invasion success: a hypothesis

Our understanding of the interrelated mechanisms driving plant invasions, such as the interplay between enemy release and resource‐acquisition traits, is biased by an aboveground perspective. To address this bias, I hypothesize that plant release from belowground enemies (especially fungal pathogens) will give invasive plant species a fitness advantage in the alien range, via shifts in root traits (e.g., increased specific root length and branching intensity) that increase resource uptake and competitive ability compared to native species in the alien range, and compared to plants of the invader in its native range. Such root‐trait changes could be ecological or evolutionary in nature. I explain how shifts in root traits could occur as a consequence of enemy release and contribute to invasion success of alien plants, and how they could be interrelated with other potential belowground drivers of invasion success (allelopathy, mutualist enhancement). Finally, I outline the approaches that could be taken to test whether belowground enemy release results in increased competitive ability and nutrient uptake by invasive alien plants, via changes in root traits in the alien range.     

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.     

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.     

不同干扰条件下枸杞园节肢动物群落结构与动态

2008年通过对宁夏银川地区不同干扰条件下枸杞园节肢动物群落的系统调查,共采集节肢动物151628头,鉴定出4纲27目76科167种,其中天敌亚群落61种,化防园23种,有机园30种,自生园61种,天敌总量的比例分别为10.87%、18.78%、70.34%。通过群落结构分析,自生园丰富度、个体数均明显高于化防园和有机园,有机园均匀度、多样性较高,而化防园丰富度、个体数指数都较低,而优势集中度高。通过主分量分析表明潜叶类害虫与刺吸类害虫是不同人工干扰条件下的主要害虫,刺吸类害虫成为发展有机枸杞的重要障碍,食花果类害虫具有较大的危害潜力;寄生类天敌、病原类天敌为自生园优势天敌,捕食类天敌是有机园、化防园的优势天敌,但化防园天敌作用较为微弱。自生园天敌亚群落与害虫亚群落第一对典型变量为V1=0.048x1-0.2533x2+0.5951x3+0.5207x4,W1=0.9021y1+0.0354y2+0.0223y3+0.1847y4-0.0591y5,相关系数为0.8635,化防园、有机园天敌亚群落与害虫亚群落第一对典型变量的相关系数分别为0.6826、0.7332。通过害虫-天敌亚群落的种群消长动态表明,天敌亚群落作为整体对害虫发挥着调控作用,自生园7-9月份寄生性天敌对刺吸式害虫的跟随作用很强,有机园较弱,化防园则不明显。     

Interactions between resource availability and enemy release in plant invasion

Understanding why some exotic species become invasive is essential to controlling their populations. This review discusses the possibility that two mechanisms of invasion, release from natural enemies and increased resource availability, may interact. When plants invade new continents, they leave many herbivores and pathogens behind. Species most regulated by enemies in their native range have the most potential for enemy release, and enemy regulation may be strongest for high-resource species. High resource availability is associated with low defence investment, high nutritional value, high enemy damage and consequently strong enemy regulation. Therefore, invasive plant species adapted to high resource availability may also gain most from enemy release. Strong release of high-resource species would predict that: (i) both enemy release and resources may underlie plant invasion, leading to potential interactions among control measures; (ii) increases in resource availability due to disturbance or eutrophication may increase the advantage of exotic over native species; (iii) exotic species will tend to have high-resource traits relative to coexisting native species; and (iv) although high-resource plants may experience strong enemy release in ecological time, well-defended low-resource plants may have stronger evolutionary responses to the absence of enemies.     

Non-native Microstegium vimineum populations collapse with fungal leaf spot disease outbreak

Non-native plants may meet little resistance in the novel range if they leave their biological enemies at home. As a result, species invasion can be rapid and appear unlimited. However, with time, organisms may acquire novel enemies in the novel range, or home-range enemies also may colonize the novel range. For plants, several authors have suggested that enemy release may give way to enemy acquisition in which pathogens accumulate and suppresses non-native plants. The ‘naturalization’ that occurs with acquired enemies may take decades to develop, yet most species invasion research lasts less than 4 years, and data tracking plant invasion before and after the appearance of pathogens are rare. Microstegium vimineum is an Asian grass that has invaded deciduous forest habitats in the southern Midwestern and Southeastern USA and is currently expanding in the Northeastern USA. We recorded widespread expansions in M. populations in North Carolina and Georgia (USA) between 2009 and 2011 but noticed that a fungal pathogen (indicated by leaf lesions; Bipolaris sp.) appeared on several of the populations in 2011. In 2019, we re-sampled these populations to determine whether the appearance of the fungal pathogen corresponded with a suppression of M. vimineum expansion. We found the once-expanding M. vimineum populations in retreat in 2019, and the plant population contractions were greater (and seed production lesser) where the fungal leaf spot disease was most extensive. These results suggest that enemy acquisition suppressed an active non-native plant invasion. We also found that where M. vimineum populations declined (or disappeared) native plants appeared to fill in the gap. Hence, whereby exotic species may gain advantage in novel habitat with the loss of their native-range pathogens, with longer time spans, enemy release may give way to enemy acquisition and native populations may recover if they are immune to the pathogens.

     

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.     

Climate warming affects biological invasions by shifting interactions of plants and herbivores

Plants and herbivorous insects can each be dramatically affected by temperature. Climate warming may impact plant invasion success directly but also indirectly through changes in their natural enemies. To date, however, there are no tests of how climate warming shifts the interactions among invasive plants and their natural enemies to affect invasion success. Field surveys covering the full latitudinal range of invasive Alternanthera philoxeroides in China showed that a beetle introduced for biocontrol was rare or absent at higher latitudes. In contrast, plant cover and mass increased with latitude. In a 2‐year field experiment near the northern limit of beetle distribution, we found the beetle sustained populations across years under elevated temperature, dramatically decreasing A. philoxeroides growth, but it failed to overwinter in ambient temperature. Together, these results suggest that warming will allow the natural enemy to expand its range, potentially benefiting biocontrol in regions that are currently too cold for the natural enemy. However, the invader may also expand its range further north in response to warming. In such cases where plants tolerate cold better than their natural enemies, the geographical gap between plant and herbivorous insect ranges may not disappear but will shift to higher latitudes, leading to a new zone of enemy release. Therefore, warming will not only affect plant invasions directly but also drive either enemy release or increase that will result in contrasting effects on invasive plants. The findings are also critical for future management of invasive species under climate change.     

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.     

Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors

Biological invasion is a widespread, but poorly understood phenomenon. Elton's hypothesis, supported by theory, experiment, and anecdotal evidence, suggests that an important determinant of invasion success is resident biodiversity, arguing that high diversity increases the competitive environment of communities and makes them more difficult to invade. Observational studies of plant invasions, however, find little support for this hypothesis and argue strongly against it. Lack of control of extrinsic factors (e.g., disturbance, climate, or soil fertility) that covary with biodiversity and invasion in observational studies makes it difficult to determine if their findings truly refute Elton's hypothesis. We examined performance of Crepis tectorum (an invasive, annual composite weed) in experimental prairie grassland plots and greenhouse plant assemblages in which resident species richness was directly manipulated. Under these conditions, unlike observational studies, no covarying extrinsic factors could interfere with interpreting results. We found a strong inverse association between resident diversity and invader performance as predicted by Elton's hypothesis. Higher resident diversity increased crowding, decreased available light, and decreased available nutrients all of which increased the competitive environment of diverse plant assemblages and reduced C. tectorum success. Examination of individual resident species impacts on C. tectorum performance demonstrated that this diversity effect was not due to the sampling effect. These results suggest that both Elton's hypothesis and its competitive mechanism may operate in nature, but covarying extrinsic factors may obscure the negative impact of diversity on invader success.     

Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations

Inbreeding and enemy infestation are common in plants and can synergistically reduce their performance. This inbreeding ×environment (I × E) interaction may be of particular importance for the success of plant invasions if introduced populations experience a release from attack by natural enemies relative to their native conspecifics. Here, we investigate whether inbreeding affects plant infestation damage, whether inbreeding depression in growth and reproduction is mitigated by enemy release, and whether this effect is more pronounced in invasive than native plant populations. We used the invader Silene latifolia and its natural enemies as a study system. We performed two generations of experimental out‐ and inbreeding within eight native (European) and eight invasive (North American) populations under controlled conditions using field‐collected seeds. Subsequently, we exposed the offspring to an enemy exclusion and inclusion treatment in a common garden in the species’ native range to assess the interactive effects of population origin (range), breeding treatment, and enemy treatment on infestation damage, growth, and reproduction. Inbreeding increased flower and leaf infestation damage in plants from both ranges, but had opposing effects on fruit damage in native versus invasive plants. Inbreeding significantly reduced plant fitness; whereby, inbreeding depression in fruit number was higher in enemy inclusions than exclusions. This effect was equally pronounced in populations from both distribution ranges. Moreover, the magnitude of inbreeding depression in fruit number was lower in invasive than native populations. These results support that inbreeding has the potential to reduce plant defenses in S. latifolia, which magnifies inbreeding depression in the presence of enemies. However, future studies are necessary to further explore whether enemy release in the invaded habitat has actually decreased inbreeding depression and thus facilitated the persistence of inbred founder populations and invasion success.     

Competitive displacement or biotic resistance? Disentangling relationships between community diversity and invasion success of tall herbs and shrubs

Questions: Are negative invasion–diversity relationships due to biotic resistance of the invaded plant community or to post‐invasion displacement of less competitive species? Do invasion–diversity relationships change with habitat type or resident traits? Location/species: Lowlands and uplands of western and southern Germany, Heracleum mantegazzianum; mountain range in central Germany, Lupinus polyphyllus; and coastal dunes of northwest Germany, Rosa rugosa. Methods: We tested the significance and estimated regression slopes of invasion–diversity relationships using generalized linear (mixed effects) models relating invader cover and habitat type to species richness in different plant groups, stratified based on size, life cycle and community association. Results: We found negative, positive and neutral relationships between invader cover and species richness. There were negative linear correlations of invader cover with small plant species throughout, but no negative linear correlation with tall species. Invasion–diversity relationships tended to be more negative in early‐successional habitats, such as dunes or abandoned grasslands, than in late‐successional habitats. Conclusions: Invasion diversity–relationships are complex; they vary among habitat types and among different groups of resident species. Negative invasion–diversity relationships are due to asymmetric competitive displacement of inferior species and not due to biotic resistance. Small species are displaced in early‐successional habitats, while there is little effect on persistence of tall species.     

CLONAL VARIATION AND COVARIATION IN APHID RESISTANCE TO PARASITOIDS AND A PATHOGEN

Abstract The potential rate of evolution of resistance to natural enemies depends on the genetic variation present in the population and any trade-offs between resistance and other components of fitness. We measured clonal variation and covariation in pea aphids ( Acyrthosiphon pisum ) for resistance to two parasitoid species ( Aphidius ervi and A. eadyi ) and a fungal pathogen ( Erynia neoaphidis ). We found significant clonal variation in resistance to all three natural enemies. We tested the hypothesis that there might be trade-offs (negative covariation) in defensive ability against different natural enemies, but found no evidence for this. All correlations in defensive ability were positive, that between the two parasitoid species significantly so. Defensive ability was not correlated with fecundity. A number of aphid clones were completely resistant to one parasitoid ( A. eadyi ), but a subset of these failed to reproduce subsequently. We discuss the factors that might maintain clonal variation in natural enemy resistance.     

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.     

Interactions among mutualism,competition, and predation foster species coexistence in diverse communities

In natural systems, organisms are simultaneously engaged in mutualistic, competitive, and predatory interactions. Theory predicts that species persistence and community stability are feasible when the beneficial effects of mutualisms are balanced by density-dependent negative feedbacks. Enemy-mediated negative feedbacks can foster plant species coexistence in diverse communities, but empirical evidence remains mixed. Disparity between theoretical expectations and empirical results may arise from the effects of mutualistic mycorrhizal fungi. Here, we build a multiprey species/predator model combined with a bidirectional resource exchange system, which simulates mutualistic interactions between plants and fungi. To reach population persistence, (1) the per capita rate of increase of all plant population must exceed the sum of the negative per capita effects of predation, interspecific competition, and costs of mycorrhizal association, and (2) the per capita numerical response of enemies to mycorrhizal plants must exceed the magnitude of the per capita enemy rate of mortality. These conditions reflect the balance between regulation and facilitation in the system. Interactions between plant natural enemies and mycorrhizal fungi lead to shifts in the strength and direction of net mycorrhizal effects on plants over time, with common plant species deriving greater benefits from mycorrhizal associations than rare plant species.     

Release from herbivory does not confer invasion success for Eugenia uniflora in Florida

One of the most commonly cited hypotheses explaining invasion success is the enemy release hypothesis (ERH), which maintains that populations are regulated by coevolved natural enemies where they are native but are relieved of this pressure in the new range. However, the role of resident enemies in plant invasion remains unresolved. We conducted a field experiment to test predictions of the ERH empirically using a system of native, introduced invasive, and introduced non-invasive Eugenia congeners in south Florida. Such experiments are rarely undertaken but are particularly informative in tests of the ERH, as they simultaneously identify factors allowing invasive species to replace natives and traits determining why most introduced species are unsuccessful invaders. We excluded insect herbivores from seedlings of Eugenia congeners where the native and invasive Eugenia co-occur, and compared how herbivore exclusion affected foliar damage, growth, and survival. We found no evidence to support the ERH in this system, instead finding that the invasive E. uniflora sustained significantly more damage than the native and introduced species. Interestingly, E. uniflora performed better than, or as well as, its congeners in terms of growth and survival, in spite of higher damage incidence. Further, although herbivore exclusion positively influenced Eugenia seedling survival, there were few differences among species and no patterns in regard to invasion status or origin. We conclude that the ability of E. uniflora to outperform its native and introduced non-invasive congeners, and not release from insect herbivores, contributes to its success as an invader in Florida.     

Defensive insect symbiont leads to cascading extinctions and community collapse

Animals often engage in mutualistic associations with microorganisms that protect them from predation, parasitism or pathogen infection. Studies of these interactions in insects have mostly focussed on the direct effects of symbiont infection on natural enemies without studying community‐wide effects. Here, we explore the effect of a defensive symbiont on population dynamics and species extinctions in an experimental community composed of three aphid species and their associated specialist parasitoids. We found that introducing a bacterial symbiont with a protective (but not a non‐protective) phenotype into one aphid species led to it being able to escape from its natural enemy and increase in density. This changed the relative density of the three aphid species which resulted in the extinction of the two other parasitoid species. Our results show that defensive symbionts can cause extinction cascades in experimental communities and so may play a significant role in the stability of consumer‐herbivore communities in the field.