Differences in growth and herbivory damage of native and invasive kudzu (Peuraria montana var. lobata) populations grown in the native range

The invasion success of exotic plants is often attributed to escape from natural enemies in their introduced ranges and subsequent evolutionary change in resource allocation from defense to growth and reproduction. We tested this idea by comparing resistance, tolerance, and growth between native (China) and invasive (US) populations of kudzu (Peuraria montana var. lobata) exposed to natural herbivores in the native range. The percentage of foliar damage was much higher in invasive populations than in native populations, indicating that plants from invasive populations had lower resistance to herbivory. Regression of total mass on percentage of foliar damage showed no significant differences in tolerance to herbivory between native and invasive populations. However, stem diameter and mass were significantly greater in invasive populations than in native populations. Our results may suggest geographic variation in herbivory damage and plant growth among kudzu native and invasive populations, but the role of herbivores influencing kudzu invasion requires further investigation.     

From Asian curiosity to eruptive American pest: Megacopta cribraria (Hemiptera: Plataspidae) and prospects for its biological control

The kudzu bug or bean plataspid, Megacopta cribraria (Fabricius), is native to Asia where it appears to be widely distributed (although the taxonomy is not entirely clear), but is infrequently a pest of legumes. This bug appeared in 2009 in the southeastern United States, where it is closely associated with kudzu, Pueraria montana Lour. [Merr.] variety lobata [Willd.] Maesen & S. Almeida. However, the insect has become a consistent economic pest of soybeans, Glycine max (L.) Merr., and some other leguminous crops in areas where large numbers can build in kudzu, in addition to being a considerable nuisance in urban landscapes where kudzu occurs. The insect has remarkable capacity for movement and has spread rapidly from nine Georgia counties in 2009 to seven states in 2012. Despite being a nuisance in urban areas and a crop pest, high populations of the bug also reduce the biomass of kudzu, which is itself a seriously problematic invasive weed, complicating the status of M. cribraria in its expanded range. Extant predators and a pathogen in the US have been observed attacking kudzu bugs in the laboratory and field, but no parasitism of eggs or nymphs has been observed to date. A single record of parasitism of an adult kudzu bug by a tachinid fly is known from the US, but no other adult parasitism has been observed in the US or elsewhere. Extant enemies may eventually significantly reduce the bug’s populations, but at present native enemies appear to be insufficient for the task, and exotic enemies from the kudzu bug’s native range may offer the best possibility for effective biological control in the US. Based on the available literature, the best option for an importation biological control program appears to be the platygastrid egg parasitoid Paratelenomus saccharalis (Dodd) because of its apparent host specificity, intimate biological linkages with M. cribraria, and wide geographic distribution in the Eastern Hemisphere. Other natural enemies may eventually emerge as good candidates for importation, but at present P. saccharalis appears to be the most promising.     

土壤微生物对不同种源乌桕生长的影响

【背景】土壤微生物对植物成功入侵具有重要影响,研究中国本地土壤微生物对美国入侵种乌桕的净生长效应有利于进一步理解乌桕成功入侵的机理。【方法】以本地和入侵2个种源多个种群的乌桕为试验材料,通过对土壤进行灭菌处理,研究土壤微生物对不同种源乌桕幼苗生长的影响。【结果】土壤微生物对入侵种乌桕具有正效应,与本地种相比,入侵种乌桕幼苗总生物量、相对生长速度、根冠比以及总叶面积、叶面积比、比叶面积等生物学指标在新鲜土壤中均表现出明显优势。种源和土壤处理间存在交互效应的指标显示土壤微生物去除对入侵种乌桕的抑制作用更为明显。这一结果与土壤自然天敌逃逸假说相背,入侵种乌桕在一定程度上具有较本地种更强的土壤微生物利用能力,在非根际土壤微生物的作用下入侵种乌桕具有较强的生长能力和明显的竞争优势。【结论与意义】本研究证实土壤微生物可能对乌桕成功入侵具有不可忽略的作用。由于该试验在乌桕起源地进行,结合在乌桕入侵地进行的研究有助于进一步分析土壤微生物对入侵的贡献作用;研究土壤微生物与入侵植物的互作关系有助于对入侵物种进行准确预测和有效控制,减少生物入侵对生态系统功能的破坏。     

Comparison of damage to native and exotic tallgrass prairie plants by natural enemies

We surveyed the prevalence and amount of leaf damage related to herbivory and pathogens on 12 pairs of exotic (invasive and noninvasive) and ecologically similar native plant species in tallgrass prairie to examine whether patterns of damage match predictions from the enemy release hypothesis. We also assessed whether natural enemy impacts differed in response to key environmental factors in tallgrass prairie by surveying the prevalence of rust on the dominant C₄ grass, Andropogon gerardii, and its congeneric invasive exotic C₄ grass, A. bladhii, in response to fire and nitrogen fertilization treatments. Overall, we found that the native species sustain 56.4% more overall leaf damage and 83.6% more herbivore-related leaf damage when compared to the exotic species. Moreover, we found that the invasive exotic species sustained less damage from enemies relative to their corresponding native species than the noninvasive exotic species. Finally, we found that burning and nitrogen fertilization both significantly increased the prevalence of rust fungi in the native grass, while rust fungi rarely occurred on the exotic grass. These results indicate that reduced damage from enemies may in part explain the successful naturalization of exotic species and the spread of invasive exotic species in tallgrass prairie.     

Little evidence for release from herbivores as a driver of plant invasiveness from a multi‐species herbivore‐removal experiment

Enemy release is frequently posed as a main driver of invasiveness of alien species. However, an experimental multi‐species test examining performance and herbivory of invasive alien, non‐invasive alien and native plant species in the presence and absence of natural enemies is lacking. In a common garden experiment in Switzerland, we manipulated exposure of seven alien invasive, eight alien non‐invasive and fourteen native species from six taxonomic groups to natural enemies (invertebrate herbivores), by applying a pesticide treatment under two different nutrient levels. We assessed biomass production, herbivore damage and the major herbivore taxa on plants. Across all species, plants gained significantly greater biomass under pesticide treatment. However, invasive, non‐invasive and native species did not differ in their biomass response to pesticide treatment at either nutrient level. The proportion of leaves damaged on invasive species was significantly lower compared to native species, but not when compared to non‐invasive species. However, the difference was lost when plant size was accounted for. There were no differences between invasive, non‐invasive and native species in herbivore abundance. Our study offers little support for invertebrate herbivore release as a driver of plant invasiveness, but suggests that future enemy release studies should account for differences in plant size among species.     

Testing the enemy release hypothesis: a review and meta-analysis

One of the most cited hypotheses explaining the inordinate success of a small proportion of introduced plants that become pests is the ‘natural enemies hypothesis’. This states that invasive introduced plants spread rapidly because they are liberated from their co-evolved natural enemies. This hypothesis had not been properly tested until recently. Previous reviews on this topic have been narrative and vote counting in nature. In this review, we carried out quantitative synthesis and meta-analysis using existing literature on plants and their herbivores to test the different components of the enemy release hypothesis. We found supporting evidence in that (1) insect herbivore fauna richness is significantly greater in the native than introduced ranges, and the reduction is skewed disproportionally towards specialists and insects feeding on reproductive parts; and (2) herbivore damage levels are greater on native plants than on introduced invasive congeners. However, herbivore damage levels are only marginally greater for plants in native than in introduced ranges, probably due to the small numbers of this type of study. Studies quantifying herbivore impacts on plant population dynamics are too scarce to make conclusions for either comparison of plants in native vs introduced ranges or of co-occurring native and introduced congeners. For future research, we advocate that more than two-way comparisons between plants in native and introduced ranges, or native and introduced congeners are needed. In addition, the use of herbivore exclusions to quantify the impacts of herbivory on complete sets of population vital rates of native vs introduced species are highly desirable. Furthermore, three-way comparisons among congeners of native plants, introduced invasive, and introduced non-invasive plants can also shed light on the importance of enemy release. Finally, simultaneously testing the enemy release hypothesis and other competing hypotheses will provide significant insights into the mechanisms governing the undesirable success of invasive species.     

Habitat degradation and introduction of exotic plants favor persistence of invasive species and population growth of native polyphagous fruit fly pests in a Northwestern Argentinean mosaic

Expansion of agricultural land is one of the most significant human alterations to the global environment because it entails not only native habitat loss but also introduction of exotic species. These alterations affect habitat structure and arthropod dynamics, such as those among host plants, tephritid fruit flies, and their natural enemies. We compared abundance and dynamics of pest and non-pest tephritids and their natural enemies over a mosaic of habitats differing in structure, diversity and disturbance history on the Sierra de San Javier in Tucuman, Argentina. Our prediction was that conserved habitats would be more resistant to the establishment and spread of invasive tephritid species due in part to a greater abundance of natural enemies, a greater diversity of native species in the same family and trophic level, and a greater wealth of biotic interactions. We further predicted that native species with broad host ranges should be more sensitive to habitat loss yet more competitive in less disturbed habitats than generalist native and exotic species. We found that environmental degradation, and introduction and spread of exotic host plants strongly affected distribution patterns, abundance, and phenology of native and exotic tephritids. Monophagous tephritid species and several specialized parasitoids were more sensitive to habitat loss than polyphagous species and parasitoids exhibiting a wide host range. In contrast, native monophagous species and native parasitoids appeared to exclude the invasive Mediterranean fruit fly from conserved patches of native vegetation. Nevertheless, the Mediterranean fruit fly persisted in uncontested exotic host plants and thrived in highly degradeted urban landscapes.     

Interactive effects of habitat productivity and herbivore pressure on the evolution of anti-herbivore defense in invasive plant populations

The evolution of increased competitive ability (EICA) hypothesis predicts that plants released from natural enemies should evolve to become more invasive through a shift in resource allocation from defense to growth. Resource availability in the environment is widely regarded as a major determinant of defense investment and invasiveness, and thus should be incorporated into the conceptual framework of EICA. Analysis of a simple model from the optimal defense literature demonstrates that, in contrast to the EICA hypothesis, enemy release is neither sufficient nor necessary for evolution of reduced resistance among introduced plants when habitat productivity co-varies. In particular, if the invasive range is more nutrient-poor than the native range, there could be selection for more plant defenses even with enemy release.     

The invasive shrub Buddleja davidii performs better in its introduced range

It is commonly assumed that invasive plants grow more vigorously in their introduced than in their native range, which is then attributed to release from natural enemies or to microevolutionary changes, or both. However, few studies have tested this assumption by comparing the performance of invasive species in their native vs. introduced ranges. Here, we studied abundance, growth, reproduction, and herbivory in 10 native Chinese and 10 invasive German populations of the invasive shrub Buddleja davidii (Scrophulariaceae; butterfly bush). We found strong evidence for increased plant vigour in the introduced range: plants in invasive populations were significantly taller and had thicker stems, larger inflorescences, and heavier seeds than plants in native populations. These differences in plant performance could not be explained by a more benign climate in the introduced range. Since leaf herbivory was substantially reduced in invasive populations, our data rather suggest that escape from natural enemies, associated with increased plant growth and reproduction, contributes to the invasion success of B. davidii in Central Europe.     

Plant–soil biota interactions and spatial distribution of black cherry in its native and invasive ranges

One explanation for the higher abundance of invasive species in their non‐native than native ranges is the escape from natural enemies. But there are few experimental studies comparing the parallel impact of enemies (or competitors and mutualists) on a plant species in its native and invaded ranges, and release from soil pathogens has been rarely investigated. Here we present evidence showing that the invasion of black cherry (Prunus serotina) into north‐western Europe is facilitated by the soil community. In the native range in the USA, the soil community that develops near black cherry inhibits the establishment of neighbouring conspecifics and reduces seedling performance in the greenhouse. In contrast, in the non‐native range, black cherry readily establishes in close proximity to conspecifics, and the soil community enhances the growth of its seedlings. Understanding the effects of soil organisms on plant abundance will improve our ability to predict and counteract plant invasions.     

Relationships among leaf damage, natural enemy release, and abundance in exotic and native prairie plants

The Enemy Release hypothesis holds that exotic plants may have an advantage over native plants because their specialized natural enemies are absent. We tested this hypothesis by measuring leaf damage and plant abundance for naturally-occurring plants in prairies, and by removing natural enemies in an enemy exclusion experiment. We classified plants as invasive exotic, noninvasive exotic, or native, to determine if their degree of invasiveness influenced their relationships with natural enemies. Our field surveys showed that invasive exotic plants generally had significantly lower levels of foliar damage than native species while there was no consistent pattern for noninvasive exotics compared to natives. The relationship between damage and abundance was different for exotic and native plants: foliar damage decreased with increasing abundance for exotic plants while the trend was positive for native plants. While these results from the field surveys supported the Enemy Release Hypothesis, the enemy exclusion experiment did not. There was no relationship between a species?? status as exotic or native and its degree of release from herbivory. Pastinaca sativa, the invasive exotic in this experiment, experienced gains in leaf area and vegetative biomass when treated with pesticides, indicating substantial herbivore pressure in the introduced range. These results show that foliar damage may not accurately predict the amount of herbivore pressure that plants actually experience, and that the Enemy Release hypothesis is not sufficient to explain the invasiveness of P. sativa in prairies.     

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.     

An exotic species is the favorite prey of a native enemy

Although native enemies in an exotic species'' new range are considered to affect its ability to invade, few studies have evaluated predation pressures from native enemies on exotic species in their new range. The exotic prey naiveté hypothesis (EPNH) states that exotic species may be at a disadvantage because of its naïveté towards native enemies and, therefore, may suffer higher predation pressures from the enemy than native prey species. Corollaries of this hypothesis include the native enemy preferring exotic species over native species and the diet of the enemy being influenced by the abundance of the exotic species. We comprehensively tested this hypothesis using introduced North American bullfrogs (Lithobates catesbeianus, referred to as bullfrog), a native red-banded snake (Dinodon rufozonatum, the enemy) and four native anuran species in permanent still water bodies as a model system in Daishan, China. We investigated reciprocal recognition between snakes and anuran species (bullfrogs and three common native species) and the diet preference of the snakes for bullfrogs and the three species in laboratory experiments, and the diet preference and bullfrog density in the wild. Bullfrogs are naive to the snakes, but the native anurans are not. However, the snakes can identify bullfrogs as prey, and in fact, prefer bullfrogs over the native anurans in manipulative experiments with and without a control for body size and in the wild, indicating that bullfrogs are subjected to higher predation pressures from the snakes than the native species. The proportion of bullfrogs in the snakes'' diet is positively correlated with the abundance of bullfrogs in the wild. Our results provide strong evidence for the EPNH. The results highlight the biological resistance of native enemies to naïve exotic 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.     

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.     

Are exotic natural enemies an effective way of controlling invasive plants?

Classical biological control (the introduction of exotic natural enemies) is often advocated as a tool for managing invasive species. Here, we review the effectiveness of biocontrol and explore the factors that determine whether it is an appropriate response to the invasive species problem. Although there have been some successes, biocontrol is generally poorly evaluated and, in many cases, its impact is unknown. In particular, there is limited understanding of the nature of the invasive species problem and no clear targets against which 'success' can be gauged. In addition, exotic natural enemies could act as invasive species in their own right. To improve the role of biocontrol in invasive species management, we need a better ecological understanding of the impacts of both the biocontrol agents and the target invasive species.     

Increased performance of Cirsium arvense from the invasive range

The Evolution of Increased Competitive Ability (EICA) hypothesis suggests that plants from the invasive range should perform better than plants of the same species from the native range. To properly test this, we need to compare growth of plants from the two ranges in a common environment. Ideally, all the natural enemies should be excluded, to make sure that the differences are not due to different response of plants from the two ranges to the natural enemies. We used the above design to examine the difference in growth and reproduction in Cirsium arvense plants from the invasive (North America) and native range (Europe). To account for possible differences within the ranges, we used plants from two regions, separated by at least 1000 km, in each range. Because the higher performance of species from the invasive range can be caused by their higher ability to acquire resources we compared growth of the plants in two different nutrient levels. The results indicate that plants from the invasive range are larger in most size parameters as well as parameters more closely related to fitness. For aboveground biomass, the response of plants from the invasive range to nutrient addition was weaker than that of plants from the native range and the difference between the ranges was stronger in the nutrient poor substrate. The results are in agreement with the EICA hypothesis and suggest that plants from the invasive range have higher ability to use resources and are thus able to perform well also in nutrient poor conditions.     

Prey naïveté rather than enemy release dominates the relation of an invasive spider toward a native predator

Ecosystems may suffer from the impact of invasive species. Thus, understanding the mechanisms contributing to successful invasions is fundamental for limiting the effects of invasive species. Most intuitive, the enemy release hypothesis predicts that invasive species might be more successful in the exotic range than resident sympatric species owing to the absence of coevolution with native enemies. Here, we test the enemy release hypothesis for the invasion of Europe by the North American spider Mermessus trilobatus. We compare the susceptibility of invasive Mermessus trilobatus and a native species with similar life history to a shared predator with which both species commonly co‐occur in Europe. Contrary to our expectations, invasive Mermessus trilobatus were consumed three times more frequently by native predators than their native counterparts. Our study shows that invasive Mermessus trilobatus is more sensitive to a dominant native predator than local sympatric species. This suggests that the relation between the invasive spider and its native predator is dominated by prey naïveté rather than enemy release. Further studies investigating evolutionary and ecological processes behind the invasion success of Mermessus trilobatus, including testing natural parasites and rapid reproduction, are needed to explain its invasion success in Europe.     

Comparison of phototrophic shell-degrading endoliths in invasive and native populations of the intertidal mussel Mytilus galloprovincialis

The intertidal mussel Mytilus galloprovincialis is a successful invader worldwide. Since its accidental introduction onto the South African west coast in the late 1970s, it has become the most successful marine invasive species in South Africa. One possible explanation for this phenomenon is that M. galloprovincialis suffers less from phototrophic shell-degrading endoliths in its invasive than in its native range. We assessed photoautotrophic endolithic pressure on M. galloprovincialis in native (Portugal) and invasive (South Africa) ranges. Invasive populations were more heavily infested than native populations. In Portugal, only the biggest/oldest mussels displayed endolithic erosion of the shell and the incidence of infestation was greater at higher shore levels where more prolonged exposure to light enhances endolith photosynthesis. In South Africa, even the smallest size classes of mussels were heavily infested throughout the shore. In Portugal, endolithic-induced mortality was observed at only one location, while in South Africa it occurred at all locations and at significantly higher rates than in Portugal. Important sub-lethal effects were detected in infested native mussels, confirming previous studies of invasive populations and suggesting an energy trade-off between shell repair and other physiological constraints. We observed a positive relationship between infestation rates and barnacle colonization on mussel shells, suggesting possible facilitation of barnacle settlement/survival by shell-boring pathogens. Identification of endoliths revealed common species between regions. However, two species were unique in the invasive range while another was unique in the native region. Different levels of endolithic infestation in the invasive and the native range were not explained by the effect of major environmental determinants (Photosynthetically Available Radiation and wave height). The results reject our initial hypothesis, indicating that invasion success of M. galloprovincialis is not simply explained by escape from its natural enemies but results from complex interactions between characteristics of the invaded community and properties of the invader.     

Invasive Mahonia plants outgrow their native relatives

Invasive populations often grow more vigorously than conspecific populations in the native range. This has frequently been attributed to evolutionary changes resulting either from founder effects, or from natural selection owing to enemy release. Another mechanism contributing to evolutionary change has largely been neglected in the past: Many invasive plant species do actually descend from cultivated plants and were therefore subject to breeding, including hybridization and artificial selection. In a common garden experiment, we compared invasive Central European populations of the ornamental shrub, Mahonia, with native populations of its putative parental species, Mahonia aquifolium and M. repens, from North America. We hypothesized that plants of invasive populations show increased growth and retained high levels of heritable variation in phenotypic traits. Indeed, invasive Mahonia plants grew larger in terms of stem length, number of leaves and above-ground biomass than either of the two native species, which did not differ significantly from each other. Since there are no hints on release of invasive Mahonia populations from natural enemies, it is likely that hybridization and subsequent selection by breeders have lead to an evolutionary increase of plant vigour in the introduced range. Further on, heritable variation was not consistently reduced in invasive populations compared with populations of the two native species. We suggest that interspecific hybridization among the Mahonia species has counteracted the harmful effects of genetic bottlenecks often associated with species introductions. Based on this case study, we conclude that, more attention has to be paid on the role of plant breeding when assessing the mechanisms behind successful plant invasions in future.