The enemy release hypothesis as a hierarchy of hypotheses

In ecology, a hypothesis is usually not discarded if a few studies reject it, as long as there are other studies supporting it. How to assess the usefulness of ecological hypotheses is therefore not straightforward. Using the enemy release hypothesis as an example, we show how creating a hierarchy of hypotheses (HoH) can help reviewing and evaluating evidence for and against an ecological hypothesis. In a HoH, a broad, overarching hypothesis branches into more specific and better testable sub‐hypotheses. The enemy release hypothesis is a major hypothesis in invasion ecology and posits that the absence of enemies in the exotic range of an alien species is a cause of its invasion success. Based on a systematic review of empirical tests of this hypothesis, we divided it into sub‐hypotheses, differentiating among 1) indicators for enemy release, 2) types of comparisons, and 3) types of enemies. We identified 176 empirical tests and weighted each test according to the number of alien species studied and the research method (experimental vs observational, field vs enclosure vs laboratory). For the broadly formulated enemy release hypothesis, we found nearly as much supporting (36%) as questioning evidence (43%). At the sub‐hypotheses level, however, we found that some sub‐hypotheses are strongly supported by empirical evidence, whereas others receive hardly any support. These differences are further emphasized for some types of habitat and focal taxonomic groups. Our findings suggest that several specific formulations (i.e. sub‐hypotheses) of the broad enemy release hypothesis are useful, whereas other formulations should be viewed more critically. In general, the approach outlined here can help evaluate major ecological hypotheses and their specific sub‐hypotheses. Our study also highlights the need for a scientific debate on how much supporting evidence is sufficient to consider an ecological hypothesis to be useful.     

Invasional meltdown: an experimental test and a framework to distinguish synergistic,additive, and antagonistic effects

The potential role of positive interactions among co-invaders is at the core of the invasional meltdown hypothesis. The interaction of non-native species could result in an exacerbation of each other’s effects. Thus, the resulting effect of multiple non-native species on ecosystems can be greater than the sum of their individual effects. We designed an analytical framework and a set of mesocosm experiments to assess the potential synergistic effects of three non-native species (Limnoperna fortunei, Astronotus crassipinnis, and Hydrilla verticillata) in a highly invaded floodplain in southern Brazil. We analyzed ecosystem, community, and population attributes in scenarios with non-natives. Our hypothesis of a synergistic effect was not supported. Even though effects of the invasive species were detected for all ecological levels, evidence indicated that these effects were additive. In addition to adding to the statement that origin (i.e., native vs. non-native status) does matter, we provide a tool to differentiate additive, synergistic, and antagonistic effects in situations with multiple invasions, and experimentally demonstrate additive effects of non-native species at different ecological levels.

     

Invasions: the perspective of diverse plant communities

Exotic plant invasions represent a threat to natural and managed ecosystems. Understanding of the mechanisms that determine why a given species may invade a given ecosystem, or why some biomes and regions seem more prone to invasions, is limited. One potential reason for this lack of progress may lie in how few studies have addressed invasion mechanisms from the point of view of the invaded community. On the other hand, the renewed debate about the relationship between ecological diversity and ecosystem stability offers the opportunity to revisit existing theory and empirical evidence, and to attempt to investigate which characteristics of plant communities, including their diversity, contribute to their invasibility. Empirical studies have shown both positive and negative relationships between species diversity of resident plant communities and their invasibility by external species. Rather than attempting to build a larger collection of case studies, research now needs to address the mechanisms underlying these relationships. Previous knowledge about the mechanisms favouring invasion needs to be coupled with community theory to form the basis of these new investigations. Modern community theory offers hypotheses and techniques to analyse the invasibility of communities depending on their diversity and other factors, such as species’ life histories and environmental variability. The body of knowledge accumulated in invasion ecology suggests that the role of disturbances, in interaction with fertility, and the importance of interactions with other trophic levels, are specific factors for consideration. In addition, it is essential for future studies to explicitly tease apart the effects of species richness per se from the effects of other components of ecological diversity, such as functional diversity (the number of functional groups) and trophic diversity (the number of interactions among trophic levels).     

Linking biodiversity to ecosystem function: implications for conservation ecology

We evaluate the empirical and theoretical support for the hypothesis that a large proportion of native species richness is required to maximize ecosystem stability and sustain function. This assessment is important for conservation strategies because sustenance of ecosystem functions has been used as an argument for the conservation of species. If ecosystem functions are sustained at relatively low species richness, then arguing for the conservation of ecosystem function, no matter how important in its own right, does not strongly argue for the conservation of species. Additionally, for this to be a strong conservation argument the link between species diversity and ecosystem functions of value to the human community must be clear. We review the empirical literature to quantify the support for two hypotheses: (1) species richness is positively correlated with ecosystem function, and (2) ecosystem functions do not saturate at low species richness relative to the observed or experimental diversity. Few empirical studies demonstrate improved function at high levels of species richness. Second, we analyze recent theoretical models in order to estimate the level of species richness required to maintain ecosystem function. Again we find that, within a single trophic level, most mathematical models predict saturation of ecosystem function at a low proportion of local species richness. We also analyze a theoretical model linking species number to ecosystem stability. This model predicts that species richness beyond the first few species does not typically increase ecosystem stability. One reason that high species richness may not contribute significantly to function or stability is that most communities are characterized by strong dominance such that a few species provide the vast majority of the community biomass. Rapid turnover of species may rescue the concept that diversity leads to maximum function and stability. The role of turnover in ecosystem function and stability has not been investigated. Despite the recent rush to embrace the linkage between biodiversity and ecosystem function, we find little support for the hypothesis that there is a strong dependence of ecosystem function on the full complement of diversity within sites. Given this observation, the conservation community should take a cautious view of endorsing this linkage as a model to promote conservation goals. Received: 2 September 1999 / Accepted: 26 October 1999     

Overestimation of establishment success of non-native birds in Hawaii and Britain

The tens rules states that 10 % of all introduced species establish and about 10 % of those species become invasive. Several studies have failed to support the tens rule. However, these studies are beset by a general weakness: many unsuccessful invasions are never reported, and without these data tests of the tens rules are inadequate. Here, using data on the establishment success of non-native birds in Hawaii and Britain and comparing these data with those from a previous study, we show that lack of information about failed species introductions, and the tendency to report species that have become invasive more than those that have not, result in an overestimate of the establishment success and invasion rates of non-native species.     

Invasive pythons,not anthropogenic stressors,explain the distribution of a keystone species

Untangling the causes of native species loss in human-modified systems is difficult and often controversial. Evaluating the impact of non-native species in these systems is particularly challenging, as additional human perturbations often precede or accompany introductions. One example is the ongoing debate over whether mammal declines within Everglades National Park (ENP) were caused by either the establishment of non-native Burmese pythons (Python molurus bivittatus) or the effects of other anthropogenic stressors. We examined the influence of both pythons and a host of alternative stressors—altered hydrology and habitat characteristics, mercury contamination and development—on the distribution of the marsh rabbit (Sylvilagus palustris), a once common mammal in ENP. Distance from the epicenter of the python invasion best explained marsh rabbit occurrence in suitable habitat patches, whereas none of the alternative stressors considered could explain marsh rabbit distribution. Estimates of the probability of marsh rabbit occurrence ranged from 0 at the python invasion epicenter to nearly 1.0 150 km from the invasion epicenter. These results support the hypothesis that invasive pythons shape the distribution of marsh rabbits in southern Florida. The loss of marsh rabbits and similar species will likely alter trophic interactions and ecosystem function within the Everglades, an internationally important hotspot of biodiversity. Further, our results suggest that non-native species can have profound impacts on mainland biodiversity.     

入侵植物的繁殖策略以及对本土植物繁殖的影响

理解入侵生物的繁殖策略是阐明生物入侵机制的一个重要方面。入侵植物常表现出一些共同的繁殖特征, 如以两性花为主的性系统、自动自交为主的繁育系统或不依赖传粉媒介的无融合生殖和无性繁殖以及高生殖投资的资源配置策略等。成功入侵的外来植物通过影响本土的传粉者, 在种群和群落水平上影响本土植物的有性繁殖, 甚至促使某些本土植物在繁殖对策和表型性状上发生快速转变。目前, 入侵植物繁殖策略及其生态效应的研究多侧重于入侵种的快速演化, 而有关外来植物与本土植物间的相互影响及其可能存在的协同适应研究还较为缺乏。探讨本土植物在外来种入侵压力下的繁殖对策和响应机制, 将丰富人们对物种间竞争、共存及群落构建等机制的深入了解。从繁殖和适应的角度探求入侵植物与本土植物之间的复杂关系, 将有助于解析生物入侵的机制及人类干扰下的物种演化规律, 也为预测和防控入侵植物提供科学依据。     

The biodiversity impacts of non-native species should not be extrapolated from biased single-species studies

The presence, diversity and abundance of non-native plant species in natural vegetation are common condition indicators used to determine conservation status, with consequences for management strategies and investment. The rationale behind non-native species metrics as condition indicators is the assumption that non-natives have negative consequences on native biodiversity and habitat condition. The case against non-native species is not so clear-cut, with some studies reporting neutral or even facilitative interactions, often depending on spatial scale. Observational and experimental evaluations of the impact of particular non-native species on biodiversity provide a vital evidence-base for general conservation management strategies. Unintentionally though, many studies that quantify the impacts of non-native species have resulted in a publication bias in which species with known impacts are selected for investigation far more often than benign species. Here we argue that meta-analyses of the impacts of individual non-native species on natives, no matter how meticulous or objective, should not be generalized beyond the set of ‘training’ species. The likelihood of such extrapolation is increased when meta-analyses are reported with little qualification as to the skewed sampling towards problematic species, and because alternative findings such as non-native assemblages having positive interactions with native biodiversity, are under-reported. To illustrate, we discuss two meta-analyses that make general conclusions from impact studies skewed towards ‘transformers’, the most extreme invaders. We warn that if generic non-native species management strategies were to be based on these conclusions, they could not only fail to meet objectives but in some instances harm native biodiversity.     

Competitive effects of non-native plants are lowest in native plant communities that are most vulnerable to invasion

Despite widespread acknowledgment that disturbance favors invasion, a hypothesis that has received little attention is whether non-native invaders have greater competitive effects on native plants in undisturbed habitats than in disturbed habitats. This hypothesis derives from the assumption that competitive interactions are more persistent in habitats that have not been recently disturbed. Another hypothesis that has received little attention is whether the effects of non-native plants on native plants vary among habitats that differ in soil fertility. We documented habitat occurrences of 27 non-native plant species and 377 native plant species encountered in numerous study plots in a broad sample of ecosystems in MS (USA). We then reviewed experimental and regression-based field studies in the scientific literature that specifically examined potential competitive (or facilitative) effects of these non-native species on native species and characterized the habitats in which effects were the greatest. As expected, the non-native species examined here in general were more likely to be associated with severely disturbed habitats than were the native species as a group. In contrast, we found that non-native species with competitive effects on natives were more likely to be associated with undisturbed habitats than with disturbed habitats. When longer term studies involving more resident species were given more weight in the analysis, competitive effects appeared to be the greatest in undisturbed habitats with low soil fertility. These results reinforce the notion that invasion is not synonymous with impact. The environmental conditions that promote invasion may limit competitive effects of invaders on native plant communities following invasion.     

Trait positions for elevated invasiveness in adaptive ecological networks

Our ability to predict the outcome of invasion declines rapidly as non-native species progress through intertwined ecological barriers to establish and spread in recipient ecosystems. This is largely due to the lack of systemic knowledge on key processes at play as species establish self-sustaining populations within the invaded range. To address this knowledge gap, we present a mathematical model that captures the eco-evolutionary dynamics of native and non-native species interacting within an ecological network. The model is derived from continuous-trait evolutionary game theory (i.e., Adaptive Dynamics) and its associated concept of invasion fitness which depicts dynamic demographic performance that is both trait mediated and density dependent. Our approach allows us to explore how multiple resident and non-native species coevolve to reshape invasion performance, or more precisely invasiveness, over trait space. The model clarifies the role of specific traits in enabling non-native species to occupy realised opportunistic niches. It also elucidates the direction and speed of both ecological and evolutionary dynamics of residing species (natives or non-natives) in the recipient network under different levels of propagule pressure. The versatility of the model is demonstrated using four examples that correspond to the invasion of (i) a horizontal competitive community; (ii) a bipartite mutualistic network; (iii) a bipartite antagonistic network; and (iv) a multi-trophic food web. We identified a cohesive trait strategy that enables the success and establishment of non-native species to possess high invasiveness. Specifically, we find that a non-native species can achieve high levels of invasiveness by possessing traits that overlap with those of its facilitators (and mutualists), which enhances the benefits accrued from positive interactions, and by possessing traits outside the range of those of antagonists, which mitigates the costs accrued from negative interactions. This ‘central-to-reap, edge-to-elude’ trait strategy therefore describes the strategic trait positions of non-native species to invade an ecological network. This model provides a theoretical platform for exploring invasion strategies in complex adaptive ecological networks.

     

Environmental stress alters native-nonnative relationships at the community scale

The invasion of natural habitats by nonnative species is affected by both native biodiversity and environmental conditions; however few tests of facilitation between native community members and nonnative species have been conducted along disturbance and stress gradients. There is strong evidence for an increase in facilitation between native plant species with increasing levels of natural environmental stress, however it is unknown whether these same positive interactions occur between nonnative invaders and native communities. I investigated the effects of natural stress on community interactions between native heathland species and nonnative species with two field studies conducted at the landscape and community scale. At the landscape scale of investigation, nonnative species richness was positively related to native species richness. At the community level, nonnative invaders experienced facilitation with natives in the most stressful zones, whereas they experienced competition with native plants in the less stressful zones of the heathlands. Due to the observational nature of the landscape scale data, it is unclear whether nonnative diversity levels are responding positively to extrinsic factors or to native biodiversity. The experimental component of this research suggests that native community members may ameliorate stressful environmental conditions and facilitate invasion into high stress areas. I present a conceptual model which is a modification of the Shea and Chesson diversity-invasibility model and includes both facilitation as well as competition between the native community and nonnative invaders at the community level, summing to an overall positive relationship at the landscape scale.     

Whole community invasions and the integration of novel ecosystems

The impact of invasion by a single non-native species on the function and structure of ecological communities can be significant, and the effects can become more drastic–and harder to predict–when multiple species invade as a group. Here we modify a dynamic Boolean model of plant-pollinator community assembly to consider the invasion of native communities by multiple invasive species that are selected either randomly or such that the invaders constitute a stable community. We show that, compared to random invasion, whole community invasion leads to final stable communities (where the initial process of species turnover has given way to a static or near-static set of species in the community) including both native and non-native species that are larger, more likely to retain native species, and which experience smaller changes to the topological measures of nestedness and connectance. We consider the relationship between the prevalence of mutualistic interactions among native and invasive species in the final stable communities and demonstrate that mutualistic interactions may act as a buffer against significant disruptions to the native community.     

The effects of landscape history and time-lags on plant invasion in Mediterranean coastal habitats

Human-driven landscape changes may promote plant invasions by increasing propagule pressure and providing favourable conditions for non-native species to establish and spread. The increase in invasion levels might not be immediate but rather exhibit a time-lag (i.e. invasion debt). Moreover, the relationship between invasion and landscape history (i.e. changes in landscape composition) might be extremely complex as it might also include extinction debts of invasive species currently in regression. In order to understand the effect of landscape history on plant invasion, we studied the invasion level in coastal plant communities affected by intense human-driven landscape alteration in the last 50 years. We identified all non-native plant species within 809 grid cells (250 × 250 m) along ~500 km of the Spanish SW coast. We tested the association of (1) non-native richness conditional on the overall presence of non-natives (at least one species), and (2) the occurrence of the most frequent non-native species, with the percentage of human land-cover categories in 1956, 1991 and 2007 using a multimodel inference approach. We used these models to project future invasion patterns in the region. We found non-native richness to be more associated with land-cover variables in 1956 than in 2007, suggesting the existence of an invasion debt, but not for the overall presence of non-natives. For most frequent species, the effects of past landscape alteration depended on the introduction pathway and the region of origin. Species used in agriculture were more related to past cropland area, while most of the species used in gardening or forestry showed higher affinity for recently altered areas. These results highlight the relevance of the species’ introduction history and landscape history in assessing future long-term invasion trends.     

Invasive and Non-Invasive Congeners Show Similar Trait Shifts between Their Same Native and Non-Native Ranges

Differences in morphological or ecological traits expressed by exotic species between their native and non-native ranges are often interpreted as evidence for adaptation to new conditions in the non-native ranges. In turn this adaptation is often hypothesized to contribute to the successful invasion of these species. There is good evidence for rapid evolution by many exotic invasives, but the extent to which these evolutionary changes actually drive invasiveness is unclear. One approach to resolving the relationship between adaptive responses and successful invasion is to compare traits between populations from the native and non-native ranges for both exotic invaders and congeners that are exotic but not invasive. We compared a suite of morphological traits that are commonly tested in the literature in the context of invasion for three very closely related species of Centaurea, all of which are sympatric in the same native and non-native ranges in Europe and North America. Of these, C. solstitialis is highly invasive whereas C. calcitrapa and C. sulphurea are not. For all three species, plants from non-native populations showed similar shifts in key traits that have been identified in other studies as important putative adaptive responses to post-introduction invasion. For example, for all three species plants from populations in non-native ranges were (i) larger and (ii) produced seeds that germinated at higher rates. In fact, the non-invasive C. calcitrapa showed the strongest trait shift between ranges. Centaurea solstitialis was the only species for which plants from the non-native range increased allocation to defensive spines, and allocated proportionally less resources to reproduction, patterns contrary to what would be predicted by theory and other empirical studies to enhance invasion. Our results suggest caution when interpreting the commonly observed increase in size and reproductive capacity as factors that cause exotics to become invaders.     

Species dynamics alter community diversity–biomass stability relationships

The relationship between community diversity and biomass variability remains a crucial ecological topic, with positive, negative and neutral diversity–stability relationships reported from empirical studies. Theory highlights the relative importance of Species–Species or Species–Environment interactions in driving diversity–stability patterns. Much previous work is based on an assumption of identical (stable) species‐level dynamics. We studied ecosystem models incorporating stable, cyclic and more complex species‐level dynamics, with either linear or non‐linear density dependence, within a locally stable community framework. Species composition varies with increasing diversity, interacting with the correlation of species' environmental responses to drive either positive or negative diversity–stability patterns, which theory based on communities with only stable species‐level dynamics fails to predict. Including different dynamics points to new mechanisms that drive the full range of diversity–biomass stability relationships in empirical systems where a wider range of dynamical behaviours are important.     

Secondary invasion: When invasion success is contingent on other invaders altering the properties of recipient ecosystems

Positive interactions between exotic species may increase ecosystem‐level impacts and potentially facilitate the entry and spread of other exotic species. Invader‐facilitated invasion success—”secondary invasion”—is a key conceptual aspect of the well‐known invasional meltdown hypothesis, but remains poorly defined and empirically underexplored. Drawing from heuristic models and published empirical studies, we explore this form of “secondary invasion” and discuss the phenomenon within the recognized conceptual framework of the determinants of invasion success. The term “secondary invasion” has been used haphazardly in the literature to refer to multiple invasion phenomena, most of which have other more accepted titles. Our usage of the term secondary invasion is akin to “invader‐facilitated invasion,” which we define as the phenomenon in which the invasion success of one exotic species is contingent on the presence, influence, and impacts of one or more other exotic species. We present case studies of secondary invasion whereby primary invaders facilitate the entry or establishment of exotic species into communities where they were previously excluded from becoming invasive. Our synthesis, discussion, and conceptual framework of this type of secondary invasion provides a useful reference to better explain how invasive species can alter key properties of recipient ecosystems that can ultimately determine the invasion success of other species. This study increases our appreciation for complex interactions following invasion and highlights the impacts of invasive species themselves as possible determinants of invasion success. We anticipate that highlighting “secondary invasion” in this way will enable studies reporting similar phenomena to be identified and linked through consistent terminology.     

Mutualistic fungus promotes plant invasion into diverse communities

Reducing the biological diversity of a community may decrease its resistance to invasion by exotic species. Manipulative experiments typically support this hypothesis but have focused mainly on one trophic level (i.e., primary producers). To date, we know little about how positive interactions among species may influence the relationship between diversity and invasibility, which suggests a need for research that addresses the question: under what conditions does diversity affect resistance to invasion? We used experimental manipulations of both plant diversity and the presence of an endophytic fungus to test whether a fungal mutualist of an invasive grass species (Lolium arundinaceum) switches the relationship between plant community diversity and resistance to invasion. Association with the fungal endophyte (Neotyphodium coenophialum) increased the ability of L. arundinaceum to invade communities with greater species diversity. In the absence of the endophyte, the initial diversity of the community significantly reduced the establishment of L. arundinaceum. However, establishment was independent of initial diversity in the presence of the endophyte. Fungal symbionts, like other key species, are often overlooked in studies of plant diversity, yet their presence may explain variation among studies in the effect of diversity on resistance to invasion.     

Ecology of invasive mosquitoes: effects on resident species and on human health

Investigations of biological invasions focus on patterns and processes that are related to introduction, establishment, spread and impacts of introduced species. This review focuses on the ecological interactions operating during invasions by the most prominent group of insect vectors of disease, mosquitoes. First, we review characteristics of non-native mosquito species that have established viable populations, and those invasive species that have spread widely and had major impacts, testing whether biotic characteristics are associated with the transition from established non-native to invasive. Second, we review the roles of interspecific competition, apparent competition, predation, intraguild predation and climatic limitation as causes of impacts on residents or as barriers to invasion. We concentrate on the best-studied invasive mosquito, Aedes albopictus, evaluating the application of basic ecological theory to invasions by Aedes albopictus. We develop a model based on observations of Aedes albopictus for effects of resource competition and predation as barriers to invasion, evaluating which community and ecosystem characteristics favour invasion. Third, we evaluate the ways in which invasive mosquitoes have contributed to outbreaks of human and animal disease, considering specifically whether invasive mosquitoes create novel health threats, or modify disease transmission for existing pathogen-host systems.     

Non-Native Plant Invasion along Elevation and Canopy Closure Gradients in a Middle Rocky Mountain Ecosystem

Mountain environments are currently among the ecosystems least invaded by non-native species; however, mountains are increasingly under threat of non-native plant invasion. The slow pace of exotic plant invasions in mountain ecosystems is likely due to a combination of low anthropogenic disturbances, low propagule supply, and extreme/steep environmental gradients. The importance of any one of these factors is debated and likely ecosystem dependent. We evaluated the importance of various correlates of plant invasions in the Wallowa Mountain Range of northeastern Oregon and explored whether non-native species distributions differed from native species along an elevation gradient. Vascular plant communities were sampled in summer 2012 along three mountain roads. Transects (n = 20) were evenly stratified by elevation (~70 m intervals) along each road. Vascular plant species abundances and environmental parameters were measured. We used indicator species analysis to identify habitat affinities for non-native species. Plots were ordinated in species space, joint plots and non-parametric multiplicative regression were used to relate species and community variation to environmental variables. Non-native species richness decreased continuously with increasing elevation. In contrast, native species richness displayed a unimodal distribution with maximum richness occurring at mid–elevations. Species composition was strongly related to elevation and canopy openness. Overlays of trait and environmental factors onto non-metric multidimensional ordinations identified the montane-subalpine community transition and over-story canopy closure exceeding 60% as potential barriers to non-native species establishment. Unlike native species, non-native species showed little evidence for high-elevation or closed-canopy specialization. These data suggest that non-native plants currently found in the Wallowa Mountains are dependent on open canopies and disturbance for establishment in low and mid elevations. Current management objectives including restoration to more open canopies in dry Rocky Mountain forests, may increase immigration pressure of non-native plants from lower elevations into the montane and subalpine zones.     

Biotic resistance to invasion is ubiquitous across ecosystems of the United States

The biotic resistance hypothesis predicts that diverse native communities are more resistant to invasion. However, past studies vary in their support for this hypothesis due to an apparent contradiction between experimental studies, which support biotic resistance, and observational studies, which find that native and non‐native species richness are positively related at broad scales (small‐scale studies are more variable). Here, we present a novel analysis of the biotic resistance hypothesis using 24 456 observations of plant richness spanning four community types and seven ecoregions of the United States. Non‐native plant occurrence was negatively related to native plant richness across all community types and ecoregions, although the strength of biotic resistance varied across different ecological, anthropogenic and climatic contexts. Our results strongly support the biotic resistance hypothesis, thus reconciling differences between experimental and observational studies and providing evidence for the shared benefits between invasive species management and native biodiversity conservation.