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

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

Conflicting values: ecosystem services and invasive tree management

Tree species have been planted widely beyond their native ranges to provide or enhance ecosystem services such as timber and fibre production, erosion control, and aesthetic or amenity benefits. At the same time, non-native tree species can have strongly negative impacts on ecosystem services when they naturalize and subsequently become invasive and disrupt or transform communities and ecosystems. The dichotomy between positive and negative effects on ecosystem services has led to significant conflicts over the removal of non-native invasive tree species worldwide. These conflicts are often viewed in only a local context but we suggest that a global synthesis sheds important light on the dimensions of the phenomenon. We collated examples of conflict surrounding the control or management of tree invasions where conflict has caused delay, increased cost, or cessation of projects aimed at invasive tree removal. We found that conflicts span a diverse range of taxa, systems and countries, and that most conflicts emerge around three areas: urban and near-urban trees; trees that provide direct economic benefits; and invasive trees that are used by native species for habitat or food. We suggest that such conflict should be seen as a normal occurrence in invasive tree removal. Assessing both positive and negative effects of invasive species on multiple ecosystem services may provide a useful framework for the resolution of conflicts.     

Challenges and trade-offs in the management of invasive alien trees

Over 430 alien tree species worldwide are known to be invasive, and the list is growing as more tree species are moved around the world and become established in novel environments. Alien trees can simultaneously bring many benefits and cause substantial environmental harm, very often leading to conflicts over how they should be managed. The impacts grow over time as invasions spread, and societal perceptions of the value of alien trees also change as understanding grows and as values shift. This leads to a dynamic environment in which trade-offs are required to maximise benefits and minimise harm. The management of alien tree populations needs to be strategic and adaptive, combining all possible management interventions to promote the sustainable delivery of optimal outcomes. We use examples, mainly from South Africa (where issues relating to invasive alien trees introduced for forestry have received most attention), to argue for holistic and collaborative approaches to alien tree management. Such approaches need to include bold steps, such as phasing out unsustainable plantation forestry that is based on highly invasive species, and in which the costs are externalised. Furthermore, it would be advisable to impose much stricter controls on the introduction of alien trees to new environments, so that problems that would arise from subsequent invasions can be avoided.     

Understanding the establishment success of non-indigenous fishes: lessons from population genetics

During the last 10 years, an increasing number of studies have explored evolutionary aspects of biological invasions. It is becoming increasingly clear that evolutionary processes play an important role during the establishment of non-native species. Genetic drift during the colonization process followed by strong selection imposed through a change in biotic conditions and co-evolutionary disequilibrium set the conditions for rapid evolutionary change in introduced populations. Different hypotheses, which have been proposed to explain how evolutionary and genetic processes, can facilitate invasiveness are explored and their relevance for fish invasions is discussed. Empirical evidence increasingly suggests that admixture after multiple introductions, hybridization between native and non-native species and enemy release can all catalyse the evolution of invasiveness. A number of studies also suggest that genetic bottlenecks might represent less of genetic paradox than previously thought. Much of the theoretical developments and empirical evidence concerning the importance of evolution during biological invasions has been provided from studies on invasive plants. Despite their prominence, fish invasions have received little attention from evolutionary biologists. Recent advances in population genetic analysis such as non-equilibrium methods and genomic techniques such as microarray technology provide suitable tools to address such issues.     

Livestock reduces juvenile tree growth of alien invasive species with a minimal effect on natives: a field experiment using exclosures

Many alien invasive tree species were originally introduced to their non-native ranges for use in forestry and as urban trees. These alien species were selected for their fast growth and not necessarily for possessing mechanisms which deter browsing. Instead, many tree species native to semiarid areas of the world evolved mechanisms which deter browsing, presumably at the cost of slower growth. In a semiarid rangeland we observed that livestock exclusion greatly promoted the growth of juveniles of several alien species but not of native species, and we hypothesized that this increase in growth of aliens was due to livestock preference for alien and not native trees. With the objective of quantifying our observations and understanding the mechanism underlying the increased growth rates of alien juvenile trees under livestock exclusion, we assessed growth and browsing levels in juveniles of two alien invasive and four abundant native tree species within three parcels where livestock was excluded and three parcels with livestock at 0.20 cattle equivalents.ha^?1. Alien species grew around four-fold faster under livestock exclusion than with livestock and, as predicted, received five times more browsing than natives. Instead, native species did not significantly increase their growth rate with livestock exclusion. The results support our hypothesis and the implications for management would be that stocking paddocks with livestock to browse existing alien juveniles and re-growth of felled adults should be effective in delaying invasions of trees used for forestry without significantly affecting the growth of the most abundant native trees.     

Intercontinental biotic invasions: what can we learn from native populations and habitats?

The effectiveness of management strategies for invasive species is often hampered by a lack of clear understanding of the factors that limit species distributions. The distribution of exotic species, especially those that are invasive, are often so dynamic that limiting factors are difficult to identify. Comparisons of exotic species between their native ranges, where they are presumably close to equilibrium with controlling factors, and their ranges in areas of introduction can circumvent this difficulty. Such studies would help identify (1) limiting factors for distributions in native ranges, (2) factors associated with a high degree of invasiveness, (3) changes in genetics and morphology since introduction, which also might contribute to invasiveness, and (4) future directions and rates of invasion as a basis for developing detection/warning systems. Findings from such comparative studies would be highly valuable for understanding the dynamics of biological invasions and for improving the effectiveness of management to prevent or control invasives.     

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

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

The naturalization to invasion transition: Are there introduction‐history correlates of invasiveness in exotic plants of Australia?

Of the large number of exotic plant species that become naturalized in new geographic regions, only a subset make the transition to become invasive. Identifying the factors that underpin the transition from naturalization to invasion is important for our understanding of biological invasions. To determine introduction‐history correlates of invasiveness among naturalized plant species of Australia, we compared geographic origin, reason for introduction, minimum residence time and growth form between naturalized non‐invasive species and naturalized invasive plant species. We found that more invasive species than expected originated from South America and North America, while fewer invasive species than expected originated from Europe and Australasia. There was no significant difference between invasive and non‐invasive species with respect to reason for introduction to Australia. However, invasive species were significantly more likely to have been resident in Australia for a longer period of time than non‐invasive species. Residence times of invasive species were consistently and significantly higher than residence times of non‐invasive species even when each continent of origin was considered separately. Furthermore, residence times for both invasive and non‐invasive species varied significantly as a function of continent of origin, with species from South America having been introduced to Australia more recently on average than species from Europe, Australasia and North America. We also found that fewer invasive species than expected were herbs and more invasive species than expected were primarily climbers. Considered together, our results indicate a high propensity for invasiveness in Australia among exotic plant species from South America, given that they appear in general capable of more rapid shifts to invasiveness than aliens from other regions. Furthermore, our findings support an emerging global generality that introduction‐history traits must be statistically controlled for in comparative studies exploring life‐history and ecological correlates of invasion success.     

Invasive alien plants in China: role of clonality and geographical origin

Biological invasions have become a significant threat to the global environment. Unfortunately, to date there is no consensus on invasion mechanisms and predictive models. Controversies range from whether we can reliably predict which species may become invasive to which species characteristics (e.g., life history, taxonomic groups, or geographic origin) contribute to the invasion processes. We examined 126 invasive alien plant species in China to understand the role of clonality and geographical origin in their invasion success. These species were categorized into three groups (I, II, III) based on their invasiveness in terms of current spatial occupation and the degree of damage to invaded habitats. Clonal plants consisted of almost half (44%) of the 126 invasive species studied, and consisted of 66% of 32 the most invasive alien plant species (Group I). There was a significant positive relationship between clonality and species invasiveness. A 68% of the 126 species studied originated in the continent of America (North and/or South America). These preliminary findings support that America is the primary geographical origin of invasive alien plant species in China and that clonality of the invasive plant species contributed significantly to the their invasiveness. The results suggest an urgent need at the global scale to investigate the mechanisms whereby plant clonal growth influences plant invasions, and the need for a focus at regional scale to examine factors affecting the exchange of invasive plant species between America and China.     

Biological invasions increase the richness of arbuscular mycorrhizal fungi from a Hawaiian subtropical ecosystem

Biological invasions can have various impacts on the diversity of important microbial mutualists such as mycorrhizal fungi, but few studies have tested whether the effects of invasions on mycorrhizal diversity are consistent across spatial gradients. Furthermore, few of these studies have taken place in tropical ecosystems that experience an inordinate rate of invasions into native habitats. Here, we examined the effects of plant invasions dominated by non-native tree species on the diversity of arbuscular mycorrhizal (AM) fungi in Hawaii. To test the hypothesis that invasions result in consistent changes in AM fungal diversity across spatial gradients relative to native forest habitats, we sampled soil in paired native and invaded sites from three watersheds and used amplicon sequencing to characterize AM fungal communities. Whether our analyses considered phylogenetic relatedness or not, we found that invasions consistently increased the richness of AM fungi. However, AM fungal species composition was not related to invasion status of the vegetation nor local environment, but stratified by watershed. Our results suggest that while invasions can lead to an overall increase in the diversity of microbial mutualists, the effects of plant host identity or geographic structuring potentially outweigh those of invasive species in determining the community membership of AM fungi. Thus, host specificity and spatial factors such as dispersal need to be taken into consideration when examining the effects of biological invasions on symbiotic microbes.     

Naturalization of introduced plants: ecological drivers of biogeographical patterns

CONTENTS: Summary 383 I. Introduction 383 II. The introduction-naturalization-invasion continuum for conceptualizing biological invasions 384 III. The biogeographical background for studying naturalization: variation among populations and regions 385 IV. Factors determining naturalization in plants 388 Acknowledgements 392 References 392 SUMMARY: The literature on biological invasions is biased in favour of invasive species - those that spread and often reach high abundance following introduction by humans. It is, however, also important to understand previous stages in the introduction-naturalization-invasion continuum ('the continuum'), especially the factors that mediate naturalization. The emphasis on invasiveness is partly because most invasions are only recognized once species occupy large adventive ranges or start to spread. Also, many studies lump all alien species, and fail to separate introduced, naturalized and invasive populations and species. These biases impede our ability to elucidate the full suite of drivers of invasion and to predict invasion dynamics, because different factors mediate progression along different sections of the continuum. A better understanding of the determinants of naturalization is important because all naturalized species are potential invaders. Processes leading to naturalization act differently in different regions and global biogeographical patterns of plant invasions result from the interaction of population-biological, macroecological and human-induced factors. We explore what is known about how determinants of naturalization in plants interact at various scales, and how their importance varies along the continuum. Research that is explicitly linked to particular stages of the continuum can generate new information that is appropriate for improving the management of biological invasions if, for example, potentially invasive species are identified before they exert an impact.     

洲际入侵植物生态位稳定性研究进展

人类活动引起的大规模洲际物种交换与生物入侵, 改变了当地生态系统结构与功能, 使生物多样性受到日益严重的威胁。本文通过综合分析主要国家和地区入侵植物的地理起源, 发现洲际入侵主要包括东亚—北美、东亚—南美、欧洲—南非、欧洲—北美、欧洲—东亚、北美—大洋洲等, 这些洲际入侵造成的后果往往比陆内入侵更为严重。利用物种分布模型(SDMs)预测入侵物种潜在分布范围是有效管理和提早预防生物入侵的重要依据, 但这些模型的一个关键假定是: 入侵物种的生态位在空间和时间上是保守的、稳定的。然而, 对于远离原产地种群并能快速适应新生境的洲际入侵植物来说, 生态位可能发生显著的变化。入侵种能否在入侵地保持原有的生态位, 取决于制约其生态分布的限制因素和生态过程在不同地区间是否发生变化。本文中作者总结了洲际入侵与陆内入侵的生态与进化过程的异同点, 认为这些限制物种原产地分布的因素如扩散限制、种间互作、适应性进化、生态可塑性和种群遗传特性等均可能导致入侵物种生态位的改变。建议下一步的研究应该重视: (1)对生态位属性进行多尺度的研究, 包括时间、空间、环境或系统发育等几个方面; (2)对比生态位稳定与发生偏移的物种特性, 确定什么样的入侵物种更容易改变原有的生态位; (3)进行生态位时间动态格局研究, 探讨生态位变化的倾向、历史速率和偏移程度, 以便判定生态位变化趋势。这些研究结果将会进一步提高物种分布模型的预测能力, 有助于更为准确地揭示气候变化和物种入侵对生物多样性的影响。     

Seedling growth rate and survival do not predict invasiveness in naturalized woody plants in New Zealand

We tested if plant species invasiveness (measured as rate of geographic spread in New Zealand) was positively associated with seedling relative growth rate (RGR) and survival, among 33 naturalized woody plant species in four families (Fabaceae, Mimosaceae, Pinaceae, Rosaceae). Eight disturbance and fertilization treatments were applied to seedlings in pots to mimic conditions the species are likely to encounter in the wild. We tested if seedlings of more invasive species have higher RGR and greater survival under these conditions. We also tested whether more invasive species had wider tolerance of the conditions to which they were subjected. There were no significant relationships between seedling RGR or survival and invasiveness for any of the treatments. Measures of tolerance (a species' relative performance across all treatments), based on both RGR and survival, also failed to explain differences in invasiveness. Our findings contrast with those from a recent study by Grotkopp et al. (2002) showing a positive correlation between seedling RGR and invasiveness in Pinus species, even though our study included 12 Pinus species. The findings of the two studies may differ because they focus on different stages in the invasion process. Our study tested whether RGR (and survival) was associated with the rate of spread of invasive species following naturalization, whereas Grotkopp et al. primarily tested whether RGR was associated with the probability of naturalization. We caution that relationships between RGR and measures of invasiveness are likely to be confounded with human introduction effort. Among pines, species with high RGR are more likely to have been widely cultivated, for purposes such as timber production, providing more opportunities for naturalization and spread. Associations between RGR, invasiveness and human introduction effort need to be partitioned out before we can reliably infer causal relationships.     

Effects of clonal integration in the expansion of two alien <Emphasis Type="Italic">Carpobrotus</Emphasis> species into a coastal dune system – a field experiment

What makes a plant a successful invader is one of the most interesting questions in modern ecology. Comparative studies including congeners differing in invasiveness are a straightforward approach to detect potential traits explaining invasions. In this experiment we studied the importance of clonal integration and the capacity to buffer fragmentation in the expansion of two stoloniferous invaders, Carpobrotus edulis, considered more invasive, and Carpobrotus acinaciformis, considered less invasive. In particular we aim to determine whether differences in these clonal traits may explain differences in invasiveness between both species. We report evidence that clonal integration favour the expansion of the two exotic clonal species into a sand dune system. Benefit derived from clonal integration by itself does not explain differences in invasiveness between theses two exotic species. However, our result indicates that the greater invasiveness of C. edulis could be explained by a higher capacity to buffer the negative effect of fragmentation in comparison with C. acinaciformis. To elucidate the real contribution of clonal traits in plant invasions, new comparative studies should be conducted including more clonal species.     

Dispersal and recruitment limitation in native versus exotic tree species: life‐history strategies and Janzen‐Connell effects

Life‐history traits of invasive exotic plants are typically considered to be exceptional vis‐à‐vis native species. In particular, hyper‐fecundity and long range dispersal are regarded as invasive traits, but direct comparisons with native species are needed to identify the life‐history stages behind invasiveness. Until recently, this task was particularly problematic in forests as tree fecundity and dispersal were difficult to characterize in closed stands. We used inverse modelling to parameterize fecundity, seed dispersal and seedling dispersion functions for two exotic and eight native tree species in closed‐canopy forests in Connecticut, USA. Interannual variation in seed production was dramatic for all species, with complete seed crop failures in at least one year for six native species. However, the average per capita seed production of the exotic Ailanthus altissima was extraordinary: > 40 times higher than the next highest species. Seed production of the shade tolerant exotic Acer platanoides was average, but much higher than the native shade tolerant species, and the density of its established seedlings (≥ 3 years) was higher than any other species. Overall, the data supported a model in which adults of native and exotic species must reach a minimum size before seed production occurred. Once reached, the relationship between tree diameter and seed production was fairly flat for seven species, including both exotics. Seed dispersal was highly localized and usually showed a steep decline with increasing distance from parent trees: only Ailanthus altissima and Fraxinus americana had mean dispersal distances > 10 m. Janzen‐Connell patterns were clearly evident for both native and exotic species, as the mode and mean dispersion distance of seedlings were further from potential parent trees than seeds. The comparable intensity of Janzen‐Connell effects between native and exotic species suggests that the enemy escape hypothesis alone cannot explain the invasiveness of these exotics. Our study confirms the general importance of colonization processes in invasions, yet demonstrates how invasiveness can occur via divergent colonization strategies. Dispersal limitation of Acer platanoides and recruitment limitation of Ailanthus altissima will likely constitute some limit on their invasiveness in closed‐canopy forests.     

Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems

Although the number of studies on invasive plants and animals has risen exponentially, little is known about invasive microbes, especially non-pathogenic ones. Microbial invasions by viruses, bacteria, fungi and protists occur worldwide but are much harder to detect than invasions by macroorganisms. Invasive microbes have the potential to significantly alter community structure and ecosystem functioning in diverse terrestrial and aquatic ecosystems. Consequently, increased attention is needed on non-pathogenic invasive microbes, both free-living and symbiotic, and their impacts on communities and ecosystems. Major unknowns include the characteristics that make microbes invasive and properties of the resident communities and the environment that facilitate invasions. A comparison of microbial invasions with invasions of macroorganisms should provide valuable insights into general principles that apply to invasions across all domains of life and to taxon-specific invasion patterns. Invasive microbes appear to possess traits thought to be common in many invasive macroorganisms: high growth rate and resource utilization efficiency, and superior competitive abilities. Invading microorganisms are often similar to native species, but with enhanced performance traits, and tend to spread in lower diversity communities. Global change can exacerbate microbial invasions; therefore, they will likely increase in the future.     

A theorem for the invasion triangle and its applicability for invasion biology

The triangle conceptual model is a construct that is foundational across several fields of the natural sciences including the study of diseases, invasive species, and fire. The invasion triangle incorporates the complex ecological and evolutionary interactions between the qualities of the abiotic environment, the invader, and the biotic interactions that describes or predicts the impacts of the invasive species. Although the triangle concept is widely used among fields, to date there has not been an analytical implementation of the model. Current modelling in invasion biology often only considers the effects of one or two factors on the outcomes of species introductions. A mathematical implementation of the triangle model will allow a more comprehensive consideration of the various ecological factors. Here, we provide the first mathematical theorem for an interpretation of the invasion triangle that allows for the consideration of time. This new analytical development of the triangle is flexible, and can be used to model the spatial and temporal population dynamics observed in invasions. We also describe the conditions under which invasion is maintained when factors change with opposing effects. In this interpretation, the lower limits for invasion are explicitly defined and each component can move independently. The complexity of the interactions between factors contributing to invasions is integrated into the single model, such as those suggested by major invasion hypotheses. We briefly describe how the theorem can be applied to account for various phenomena in range dynamics using rapid range expansion and the time lag in invasions as examples. Future work can explicitly define the interdependence among components to suit more specific questions.     

Exotic Mammals Disperse Exotic Fungi That Promote Invasion by Exotic Trees

Biological invasions are often complex phenomena because many factors influence their outcome. One key aspect is how non-natives interact with the local biota. Interaction with local species may be especially important for exotic species that require an obligatory mutualist, such as Pinaceae species that need ectomycorrhizal (EM) fungi. EM fungi and seeds of Pinaceae disperse independently, so they may use different vectors. We studied the role of exotic mammals as dispersal agents of EM fungi on Isla Victoria, Argentina, where many Pinaceae species have been introduced. Only a few of these tree species have become invasive, and they are found in high densities only near plantations, partly because these Pinaceae trees lack proper EM fungi when their seeds land far from plantations. Native mammals (a dwarf deer and rodents) are rare around plantations and do not appear to play a role in these invasions. With greenhouse experiments using animal feces as inoculum, plus observational and molecular studies, we found that wild boar and deer, both non-native, are dispersing EM fungi. Approximately 30% of the Pinaceae seedlings growing with feces of wild boar and 15% of the seedlings growing with deer feces were colonized by non-native EM fungi. Seedlings growing in control pots were not colonized by EM fungi. We found a low diversity of fungi colonizing the seedlings, with the hypogeous Rhizopogon as the most abundant genus. Wild boar, a recent introduction to the island, appear to be the main animal dispersing the fungi and may be playing a key role in facilitating the invasion of pine trees and even triggering their spread. These results show that interactions among non-natives help explain pine invasions in our study area.     

Similar responses in morphology,growth, biomass allocation,and photosynthesis in invasive <Emphasis Type="Italic">Wedelia trilobata</Emphasis> and native congeners to CO<Subscript>2</Subscript> enrichment

Both global change and biological invasions threaten biodiversity worldwide. However, their interactions and related mechanisms are still not well elucidated. To elucidate potential traits contributing to invasiveness and whether ongoing increase in CO₂ aggravates invasions, noxious invasive Wedelia trilobata and native Wedelia urticifolia and Wedelia chinensis were compared under ambient and doubled atmospheric CO₂ concentrations in terms of growth, biomass allocation, morphology, and physiology. The invader had consistently higher leaf mass fraction (LMF) and specific leaf area than the natives, contributing to a higher leaf area ratio, and therefore to faster growth and invasiveness. The higher LMF of the invader was due to lower root mass fraction and higher fine root percent. On the other hand, the invader allocated a higher fraction of leaf nitrogen (N) to photosynthetic apparatus, which was associated with its higher photosynthetic rate, and resource use efficiency. All these traits collectively contributed to its invasiveness. CO₂ enrichment increased growth of all studied species by increasing actual photosynthesis, although it decreased photosynthetic capacities due to decreased leaf and photosynthetic N contents. Responses of the invasive and native plants to elevated CO₂ were not significantly different, indicating that the ongoing increase in CO₂ may not aggravate biological invasions, inconsistent with the prevailing results in references. Therefore, more comparative studies of related invasive and native plants are needed to elucidate whether CO₂ enrichment facilitates invasions.