No evidence for evolutionarily decreased tolerance and increased fitness in invasive Chromolaena odorata: implications for invasiveness and biological control

Tolerance, the degree to which plant fitness is affected by herbivory, is associated with invasiveness and biological control of introduced plant species. It is important to know the evolutionary changes in tolerance of invasive species after introduction in order to understand the mechanisms of biological invasions and assess the feasibility of biological control. While many studies have explored the evolutionary changes in resistance of invasive species, little has been done to address tolerance. We hypothesized that compared with plants from native populations, plants from invasive populations may increase growth and decrease tolerance to herbivory in response to enemy release in introduced ranges. To test this hypothesis, we compared the differences in growth and tolerance to simulated herbivory between plants from invasive and native populations of Chromolaena odorata, a noxious invader of the tropics and subtropics, at two nutrient levels. Surprisingly, flower number, total biomass (except at high nutrient), and relative increase in height were not significantly different between ranges. Also, plants from invasive populations did not decrease tolerance to herbivory at both nutrient levels. The invader from both ranges compensated fully in reproduction after 50?% of total leaf area had been damaged, and achieved substantial regrowth after complete shoot damage. This strong tolerance to damage was associated with increased resource allocation to reproductive structures and with mobilization of storage reserves in roots. The innately strong tolerance may facilitate invasion success of C. odorata and decrease the efficacy of leaf-feeding biocontrol agents. Our study highlights the need for further research on biogeographical differences in tolerance and their role in the invasiveness of exotic plants and biological control.     

Does time since introduction influence enemy release of an invasive weed?

Release from natural enemies is considered to potentially play an important role in the initial establishment and success of introduced plants. With time, the species richness of herbivores using non-native plants may increase [species-time relationship (STR)]. We investigated whether enemy release may be limited to the early stages of invasion. Substituting space for time, we sampled invertebrates and measured leaf damage on the invasive species Senecio madagascariensis Poir. at multiple sites, north and south of the introduction site. Invertebrate communities were collected from plants in the field, and reared from collected plant tissue. We also sampled invertebrates and damage on the native congener Senecio pinnatifolius var. pinnatifolius A. Rich. This species served as a control to account for environmental factors that may vary along the latitudinal gradient and as a comparison for evaluating the enemy release hypothesis (ERH). In contrast to predictions of the ERH, greater damage and herbivore abundances and richness were found on the introduced species S. madagascariensis than on the native S. pinnatifolius. Supporting the STR, total invertebrates (including herbivores) decreased in abundance, richness and Shannon diversity from the point of introduction to the invasion fronts of S. madagascariensis. Leaf damage showed the opposite trend, with highest damage levels at the invasion fronts. Reared herbivore loads (as opposed to external collections) were greater on the invader at the point of introduction than on sites further from this region. These results suggest there is a complex relationship between the invader and invertebrate community response over time. S. madagascariensis may be undergoing rapid changes at its invasion fronts in response to environmental and herbivore pressure.     

The advantages and disadvantages of being introduced

Introduced species, those dispersed outside their natural ranges by humans, now cause almost all biological invasions, i.e., entry of organisms into habitats with negative effects on organisms already there. Knowing whether introduction tends to give organisms specific ecological advantages or disadvantages in their new habitats could help understand and control invasions. Even if no specific species traits are associated with introduction, introduced species might out-compete native ones just because the pool of introduced species is very large (“global competition hypothesis”). Especially in the case of intentional introduction, high initial propagule pressure might further increase the chance of establishment, and repeated introductions from different source populations might increase the fitness of introduced species through hybridization. Intentional introduction screens species for usefulness to humans and so might select for rapid growth and reproduction or carry species to suitable habitats, all which could promote invasiveness. However, trade offs between growth and tolerance might make introduced species vulnerable to extreme climatic events and cause some invasions to be transient (“reckless invader hypothesis”). Unintentional introduction may screen for species associated with human-disturbed habitats, and human disturbance of their new habitats may make these species more invasive. Introduction and natural long-distance dispersal both imply that species have neither undergone adaptation in their new habitats nor been adapted to by other species there. These two characteristics are the basis for many well-known hypotheses about invasion, including the “biotic resistance”, “enemy release”, “evolution of increased competitive ability” and “novel weapon” hypotheses, each of which has been shown to help explain some invasions. To the extent that biotic resistance depends upon local adaption by native species, altering selection pressures could reduce resistance and promote invasion (“local adaptation hypothesis”), and restoring natural regimes could reverse this effect.     

Evolutionary increase in sexual and clonal reproductive capacity during biological invasion in an aquatic plant Butomus umbellatus (Butomaceae)

To test the hypothesis that increased allocation to reproduction is selected during biological invasion, we compared germination, survival, growth, and reproduction of native vs. introduced populations of the invasive aquatic plant Butomus umbellatus in a common greenhouse environment. Although seedling emergence and establishment did not differ consistently, survival thereafter was twice as high for eight introduced North American than eight native European populations. As predicted, introduced plants were more likely to produce sexual inflorescences and clonal asexual vegetative bulbils, and they invested much more biomass in both reproductive modes. Higher reproductive investment was due to higher proportional allocation of biomass rather than larger plant size. These results are consistent with selection for increased reproduction during range expansion. However, population genetic surveys indicate that recruitment from seed rarely occurs in introduced populations. Hence increased sexual allocation is not an adaptive response to invasion. Although increased clonal reproduction may be advantageous in expanding populations, genetic evidence from introduced populations of B. umbellatus suggests that increased clonal allocation may have arisen via stochastic processes during long-distance transport or a selective filter right at introduction, rather than incremental natural selection during range expansion.     

Invasion trajectory of alien trees: the role of introduction pathway and planting history

Global change is driving a massive rearrangement of the world's biota. Trajectories of distributional shifts are shaped by species traits, the recipient environment and driving forces with many of the driving forces directly due to human activities. The relative importance of each in determining the distributions of introduced species is poorly understood. We consider 11 Australian Acacia species introduced to South Africa for different reasons (commercial forestry, dune stabilization and ornamentation) to determine how features of the introduction pathway have shaped their invasion history. Projections from species distribution models (SDMs) were developed to assess how the reason for introduction influences the similarity between climatic envelopes in native and alien ranges. A lattice model for an idealized invasion was developed to assess the relative contribution of intrinsic traits and introduction dynamics on the abundance and extent over the course of simulated invasions. SDMs show that alien populations of ornamental species in South Africa occupy substantially different climate space from their native ranges, whereas species introduced for forestry occupy a similar climate space in native and introduced ranges. This may partly explain the slow spread rates observed for some alien ornamental plants. Such mismatches are likely to become less pronounced with the current drive towards ‘eco gardens’ resulting in more introductions of ornamental species with a close climate match between native and newly introduced regions. The results from the lattice model showed that the conditions associated with the introduction pathway (especially introduction pressure) dominate early invasion dynamics. The placement of introduction foci in urban areas limited the extent and abundance of invasive populations. Features of introduction events appear to initially mask the influence of intrinsic species traits on invasions and help to explain the relative success of species introduced for different purposes. Introduction dynamics therefore can have long‐lasting influences on the outcomes of species redistributions, and must be explicitly considered in management plans.     

Rapid evolution and range expansion of an invasive plant are driven by provenance–environment interactions

To improve our ability to prevent and manage biological invasions, we must understand their ecological and evolutionary drivers. We are often able to explain invasions after they happen, but our predictive ability is limited. Here, we show that range expansions of introduced Pinus taeda result from an interaction between genetic provenance and climate and that temperature and precipitation clines predict the invasive performance of particular provenances. Furthermore, we show that genotypes can occupy climate niche spaces different from those observed in their native ranges and, at least in our case, that admixture is not a main driver of invasion. Genotypes respond to climate in distinct ways, and these interactions affect the ability of populations to expand their ranges. While rapid evolution in introduced ranges is a mechanism at later stages of the invasion process, the introduction of adapted genotypes is a key driver of naturalisation of populations of introduced species.     

Invasion success of non-indigenous aquatic and semi-aquatic plants in their native and introduced ranges. A comparison between their invasiveness in North America and in France

Aquatic and semi-aquatic plants comprise few species worldwide, yet the introduction of non-indigenous plants represents one of the most severe examples of biological invasions. My goal is to compare the distribution and the biology of aquatic and semi-aquatic plants in their introduced ranges and in their native ranges. The primary objective of this study is to test the hypothesis that invasive species have evolved traits likely to increase their success in the new range. I made two reciprocal comparisons, i.e. I compared European species in France and in North America, and North American species in France and in North America. Twenty-seven species were classified according to their invasiveness in their introduced area. I␣found six invasive macrophyte species in France native to North America and 17 invasive species in North America native to Europe. Four species are invasive in both areas. There is no general tendency for macrophytes to be more vigorous in their introduced ranges. Most non-indigenous aquatic and semi-aquatic species are potentially invasive or widespread and well-established in their introduced country, while few species seem to be restricted in their distribution.     

Genetic differences in growth of an invasive tree species

Invasive plants are often more vigorous in their introduced ranges than in their native ranges. This may reflect an innate superiority of plants from some habitats or an escape from their enemies. Another hypothesis proposes that invasive plants evolve increased competitive ability in their introduced range. We present the results of a 14-year common garden experiment with the Chinese Tallow Tree ( Sapium sebiferum ) from its native range (Asia), place of introduction to North America (Georgia) and areas colonized a century later (Louisiana and Texas). Invasive genotypes, especially those from recently colonized areas, were larger than native genotypes and more likely to produce seeds but had lower quality, poorly defended leaves. Our results demonstrate significant post-invasion genetic differences in an invasive plant species. Post-introduction adaptation by introduced plants may contribute to their invasive success and make it difficult to predict problem species.     

Mycorrhizal associations of an invasive tree are enhanced by both genetic and environmental mechanisms

Biotic interactions involving exotic plants in their introduced ranges may differ from those of co‐occurring plant species and from interactions in their native ranges. When interactions are less negative, or more positive compared to native plant species, this may increase invasion success, and differences among ranges may cause changes in exotic plant traits. Here, we investigated arbuscular mycorrhizae (AM) associated with Triadica sebifera seedlings from populations in native (China) and introduced ranges (US) and with seedlings from US and China species within three co‐occurring genera (Liquidambar, Ulmus, Celtis) grown in multiple common gardens in both ranges. No general pattern of higher or lower AM colonization was found in the introduced range for China and US Celtis, Liquidambar, or Ulmus species. However, AM colonization was significantly higher for Triadica than for other genera, particularly in the introduced range, suggesting AM may improve Triadica's invasion success. Triadica AM colonization was higher in US than China gardens, decreased with increasing soil nitrogen in China, but was independent of soil nitrogen in the US. This might reflect a different effect of soil fertility on this mutualism among ranges. Introduced Triadica populations had higher AM colonization than native populations, particularly in US gardens, implying a possible advantage from greater AM association in the introduced range. This is the first field study demonstrating post‐introduction changes in mycorrhizal colonization of an invasive species. It indicates that there are ecological and evolutionary components to the effect of positive interactions on plant invasions.     

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.     

Evidence for the enemy release hypothesis in <Emphasis Type="Italic">Hypericum perforatum</Emphasis>

The enemy release hypothesis (ERH), which has been the theoretical basis for classic biological control, predicts that the success of invaders in the introduced range is due to their release from co-evolved natural enemies (i.e. herbivores, pathogens and predators) left behind in the native range. We tested this prediction by comparing herbivore pressure on native European and introduced North American populations of Hypericum perforatum (St Johns Wort). We found that introduced populations occur at larger densities, are less damaged by insect herbivory and suffer less mortality than populations in the native range. However, overall population size was not significantly different between ranges. Moreover, on average plants were significantly smaller in the introduced range than in the native range. Our survey supports the contention that plants from the introduced range experience less herbivore damage than plants from the native range. While this may lead to denser populations, it does not result in larger plant size in the introduced versus native range as postulated by the ERH.     

Enemy release from the effects of generalist granivores can facilitate Bromus tectorum invasion in the Great Basin Desert

The enemy release hypothesis (ERH) of plant invasion asserts that natural enemies limit populations of invasive plants more strongly in native ranges than in non‐native ranges. Despite considerable empirical attention, few studies have directly tested this idea, especially with respect to generalist herbivores. This knowledge gap is important because escaping the effects of generalists is a critical aspect of the ERH that may help explain successful plant invasions. Here, we used consumer exclosures and seed addition experiments to contrast the effects of granivorous rodents (an important guild of generalists) on the establishment of cheatgrass (Bromus tectorum) in western Asia, where cheatgrass is native, versus the Great Basin Desert, USA, where cheatgrass is exotic and highly invasive. Consistent with the ERH, rodent foraging reduced cheatgrass establishment by nearly 60% in western Asia but had no effect in the Great Basin. This main result corresponded with a region‐specific foraging pattern: rodents in the Great Basin but not western Asia generally avoided seeds from cheatgrass relative to seeds from native competitors. Our results suggest that enemy release from the effects of an important guild of generalists may contribute to the explosive success of cheatgrass in the Great Basin. These findings corroborate classic theory on enemy release and expand our understanding of how generalists can influence the trajectory of exotic plant invasions.     

The making of a rapid plant invader: genetic diversity and differentiation in the native and invaded range of Senecio inaequidens

To become invasive, exotic species have to succeed in the consecutive phases of introduction, naturalization, and invasion. Each of these phases leaves traces in genetic structure, which may affect the species’ success in subsequent phases. We examined this interplay of genetic structure and invasion dynamics in the South African Ragwort (Senecio inaequidens), one of Europe’s fastest plant invaders. We used AFLP and microsatellite markers to analyze 19 native African and 32 invasive European populations. In combination with historic data, we distinguished invasion routes and traced them back to the native source areas. This revealed that different introduction sites had markedly different success in the three invasion phases. Notably, an observed lag‐phase in Northern Germany was evidently not terminated by factors increasing the invasiveness of the resident population but by invasive spread from another introduction centre. The lineage invading Central Europe was introduced to sites in which winters are more benign than in the native source region. Subsequently, this lineage spread into areas in which winter temperatures match the native climate more closely. Genetic diversity clearly increases with population age in Europe and less clearly decreases with spread rate up to population establishment. This indicates that gene flow along well‐connected invasion routes counteracted losses of genetic diversity during rapid spread. In summary, this study suggests that multiple introductions, environmental preadaptation and high gene flow along invasion routes contributed to the success of this rapid invader. More generally, it demonstrates the benefit of combining genetic, historical, and climatic data for understanding biological invasions.     

Is invasion success explained by the enemy release hypothesis?

A recent trend in invasion ecology relates the success of non‐indigenous species (NIS) to reduced control by enemies such as pathogens, parasites and predators (i.e. the enemy release hypothesis, ERH). Despite the demonstrated importance of enemies to host population dynamics, studies of the ERH are split – biogeographical analyses primarily show a reduction in the diversity of enemies in the introduced range compared with the native range, while community studies imply that NIS are no less affected by enemies than native species in the invaded community. A broad review of the invasion literature implies at least eight non‐exclusive explanations for this enigma. In addition, we argue that the ERH has often been accepted uncritically wherever (i) NIS often appear larger, more fecund, or somehow ‘better’ than either congeners in the introduced region, or conspecifics in the native range; and (ii) known enemies are conspicuously absent from the introduced range. However, all NIS, regardless of their abundance or impact, will lose natural enemies at a biogeographical scale. Given the complexity of processes that underlie biological invasions, we argue against a simple relationship between enemy ‘release’ and the vigour, abundance or impact of NIS.     

Evidence of climatic niche shift during biological invasion

Niche-based models calibrated in the native range by relating species observations to climatic variables are commonly used to predict the potential spatial extent of species' invasion. This climate matching approach relies on the assumption that invasive species conserve their climatic niche in the invaded ranges. We test this assumption by analysing the climatic niche spaces of Spotted Knapweed in western North America and Europe. We show with robust cross-continental data that a shift of the observed climatic niche occurred between native and non-native ranges, providing the first empirical evidence that an invasive species can occupy climatically distinct niche spaces following its introduction into a new area. The models fail to predict the current invaded distribution, but correctly predict areas of introduction. Climate matching is thus a useful approach to identify areas at risk of introduction and establishment of newly or not-yet-introduced neophytes, but may not predict the full extent of invasions.     

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

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

Patterns of non-randomness in the exotic avifauna of Florida

It is now generally recognized that human-mediated biological invasion is a multistage process, successively comprising transport, introduction, establishment, and spread, and that a complete understanding of the causes of invasion requires studies of all stages. However, while many studies address the characteristics that influence establishment, relatively few address the characteristics that influence whether or not a species transits the earlier stages of transport and introduction. Here, we use data on the rich exotic avifauna of Florida to assess non-randomness in the identities of species that have passed through the transport and introduction stages. Bird species transported and introduced to Florida are non-random with respect to their taxonomic affiliations, body mass, native geographical range size, and region of origin: introductions are more likely for widespread, large-bodied species from the Neotropics and belonging to the Anatidae, Psittacidae, Ciconiidae, and Passeridae. Data on the identities of species that have attempted to breed but failed, and on the breeding population size for most established species, also allowed us to assess the extent to which the same variables influenced various aspects of post-introduction establishment. Only native geographical range size and latitudinal range mid-point distinguish between these different classes of exotic species. Geographical range size is the most general correlate of different classes of invaders in our analyses.     

The evolutionary consequences of biological invasions

A major challenge of invasion biology is the development of a predictive framework that prevents new invasions. This is inherently difficult because different biological characteristics are important at the different stages of invasion: opportunity/transport, establishment and spread. Here, we draw from recent research on a variety of taxa to examine the evolutionary causes and consequences of biological invasions. The process of introduction may favour species with characteristics that promote success in highly disturbed, human-dominated landscapes, thus exerting novel forms of selection on introduced populations. Moreover, evidence is accumulating that multiple introductions can often be critical to the successful establishment and spread of introduced species, as they may be important sources of genetic variation necessary for adaptation in new environments or may permit the introduction of novel traits. Thus, not only should the introduction of new species be prevented, but substantial effort should also be directed to preventing the secondary introduction of previously established species (and even movement of individuals among introduced populations). Modern molecular techniques can take advantage of genetic changes postintroduction to determine the source of introduced populations and their vectors of spread, and to elucidate the mechanisms of success of some invasive species. Moreover, the growing availability of genomic tools will permit the identification of underlying genetic causes of invasive success.     

飞机草入侵种群和原产地种群生长和数量型化学防御物质含量差异的比较研究

增强竞争能力的进化假说认为,在入侵地外来植物逃离了原产地天敌的控制,把原来用于防御的资源分配到生长、生殖等,从而提高竞争力。为探讨进化在恶性外来入侵植物飞机草（Chromolaena odorata）入侵中的作用,在同质种植园中的两个养分条件下比较研究了飞机草原产地和入侵地各8个种群叶片单宁含量,茎和叶片总酚、半纤维素和纤维素含量以及总生物量的差异。结果表明,在两个养分条件下,飞机草入侵种群和原产地种群总生物量差异均不显著,入侵种群茎和叶片半纤维素含量均低于原产地种群;在高养分条件下,飞机草入侵种群叶片纤维素含量低于原产地种群;在低养分条件下,入侵种群茎和叶片总酚含量高于原产地种群。由此,我们得出结论：在入侵地,飞机草未发生加快生长的进化,但数量型化学防御物质发生了遗传变化;降低的半纤维素和纤维素含量可能是对入侵地专性天敌缺乏做出进化响应的结果,提高的总酚含量有利于飞机草防御入侵地的广谱天敌。