Biotic interactions and plant invasions

Introduced plant populations lose interactions with enemies, mutualists and competitors from their native ranges, and gain interactions with new species, under new abiotic conditions. From a biogeographical perspective, differences in the assemblage of interacting species, as well as in abiotic conditions, may explain the demographic success of the introduced plant populations relative to conspecifics in their native range. Within invaded communities, the new interactions and conditions experienced by the invader may influence both its demographic success and its effects on native biodiversity. Here, we examine indirect effects involving enemies, mutualists and competitors of introduced plants, and effects of abiotic conditions on biotic interactions. We then synthesize ideas building on Darwin's idea that the kinds of new interactions gained by an introduced population will depend on its relatedness to native populations. This yields a heuristic framework to explain how biotic interactions and abiotic conditions influence invader success. We conclude that species introductions generally alter plants' interactions with enemies, mutualists and competitors, and that there is increasing evidence that these altered interactions jointly influence the success of introduced populations.     

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

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

Two tests of enemy release of commonly co-occurring bunchgrasses native in Europe and introduced in the United States

The popularly cited enemy release hypothesis, which states that non-native species are released from population control by their enemies, has not been adequately tested in plants. Many empirical studies have compared damage to native versus non-native invaders only in the invaded range, which can lead to erroneous conclusions regarding enemy release. Biogeographical studies that have compared natural enemies in native and introduced ranges have typically focused on a small area of the plants’ distributions in each range, only one plant species, and/or only one guild of natural enemies. To test enemy release, we first surveyed both pathogens and herbivores in multiple populations in both the native and naturalized ranges of three commonly co-occurring perennial bunchgrasses introduced to the United States from Europe. We then compared our field results to the number of fungal pathogens that have been documented on each species from published host-pathogen data compilations. Consistent with enemy release, our field survey showed less herbivory and denser populations in the naturalized range, but there was no evidence of release from pathogens. In contrast, the published host-pathogen data compilations produced evidence of enemy release from pathogens. The difference in results produced by the two approaches highlights the need for multiple approaches to testing mechanisms of invasions by introduced species, which can enable well supported theory to inform sound management practices.     

Stress relief may promote the evolution of greater phenotypic plasticity in exotic invasive species: a hypothesis

Invasion ecologists have often found that exotic invaders evolve to be more plastic than conspecific populations from their native range. However, an open question is why some exotic invaders can even evolve to be more plastic given that there may be costs to being plastic. Investigation into the benefits and costs of plasticity suggests that stress may constrain the expression of plasticity (thereby reducing the benefits of plasticity) and exacerbate the costs of plasticity (although this possibility might not be generally applicable). Therefore, evolution of adaptive plasticity is more likely to be constrained in stressful environments. Upon introduction to a new range, exotic species may experience more favorable growth conditions (e.g., because of release from natural enemies). Therefore, we hypothesize that any factors mitigating stress in the introduced range may promote exotic invaders to evolve increased adaptive plasticity by reducing the costs and increasing the benefits of plasticity. Empirical evidence is largely consistent with this hypothesis. This hypothesis contributes to our understanding of why invasive species are often found to be more competitive in a subset of environments. Tests of this hypothesis may not only help us understand what caused increased plasticity in some exotic invaders, but could also tell us if costs (unless very small) are more likely to inhibit the evolution of adaptive plasticity in stressful environments in general.     

Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions

Recent studies have concluded that release from native soil pathogens may explain invasion of exotic plant species. However, release from soil enemies does not explain all plant invasions. The invasion of Ammophila arenaria (marram grass or European beach grass) in California provides an illustrative example for which the enemy release hypothesis has been refuted. To explore the possible role of plant–soil community interactions in this invasion, we developed a mathematical model. First, we analyzed the role of plant–soil community interactions in the succession of A. arenaria in its native range (north-western Europe). Then, we used our model to explore for California how alternative plant–soil community interactions may generate the same effect as if A. arenaria were released from soil enemies. This analysis was carried out by construction of a 'recovery plane' that discriminates between plant competition and plant–soil community interactions. Our model shows that in California, the accumulation of local pathogens by A. arenaria could result in exclusion of native plant species. Moreover, this mechanism could trigger the rate and spatial pattern of invasive spread generally observed in nature. We propose that our 'accumulation of local pathogens' hypothesis could serve as an alternative explanation for the enemy release hypothesis to be considered in further experimental studies on invasive plant species.     

Resistance in introduced populations of a freshwater snail to native range parasites

Introduced species provide an opportunity to examine responses to novel ecological conditions, in particular to the absence of co-evolved enemies. Introduced populations could evolve lower investment in resistance or could down-regulate their immune system as a plastic response to enemy absence. The response might have consequences for the success of introduced species. Assuming a trade-off between resistance and traits related to demographic success, an evolved change or reallocation from resistance could increase the chances of invasions. On the other hand, introduced populations could have increased resistance as a correlate of greater vigour and competitive ability among successful invaders [Sampling Bias hypothesis (SBH)]. These hypotheses make different predictions about investment in resistance in introduced populations. Using a New Zealand clonal snail (Potamopyrgus antipodarum), we examined the resistance of three introduced genotypes (one from the US and two from Europe) to several populations of a native range parasite (Microphallus sp.). One genotype (Euro A) was resistant to all native range parasite populations, consistent with the SBH. However, two remaining genotypes (Euro C and US 1) were less susceptible to parasite populations that were allopatric to their source populations. Furthermore, resistance of one genotype (US 1) collected from the introduced range was indistinguishable from its resistance when collected from the range of the parasite. Hence, there was no evidence for decreased resistance in the absence of native enemies, which is inconsistent with hypotheses that envision reduced allocation to resistance or a trade-off between competitive ability and resistance.     

Response to enemies in the invasive plant Lythrum salicaria is genetically determined

Background and Aims

The enemy release hypothesis assumes that invasive plants lose their co-evolved natural enemies during introduction into the new range. This study tested, as proposed by the evolution of increased competitive ability (EICA) hypothesis, whether escape from enemies results in a decrease in defence ability in plants from the invaded range. Two straightforward aspects of the EICA are examined: (1) if invasives have lost their enemies and their defence, they should be more negatively affected by their full natural pre-invasion herbivore spectrum than their native conspecifics; and (2) the genetic basis of evolutionary change in response to enemy release in the invasive range has not been taken sufficiently into account.

Methods

Lythrum salicaria (purple loosestrife) from several populations in its native (Europe) and invasive range (North America) was exposed to all above-ground herbivores in replicated natural populations in the native range. The experiment was performed both with plants raised from field-collected seeds as well as with offspring of these where maternal effects were removed.

Key Results

Absolute and relative leaf damage was higher for introduced than for native plants. Despite having smaller height growth rate, invasive plants attained a much larger final size than natives irrespective of damage, indicating large tolerance rather than effective defence. Origin effects on response to herbivory and growth were stronger in second-generation plants, suggesting that invasive potential through enemy release has a genetic basis.

Conclusions

The findings support two predictions of the EICA hypothesis – a genetically determined difference between native and invasive plants in plant vigour and response to enemies – and point to the importance of experiments that control for maternal effects and include the entire spectrum of native range enemies.     

For or against: the importance of variation in growth rate for testing the EICA hypothesis

The evolution of increased competitive ability (EICA) hypothesis proposes that invasive species evolve decreased defense and increased competitive ability following natural enemy release. Previous studies have found evidence both for and against EICA. The resource-enemy release hypothesis (R-ERH) suggests that fast-growing species may experience stronger enemy release than slow-growing species. On the basis of R-ERH, the prediction of EICA will be held true for slow-growing genotypes, i.e., the slow-growing genotypes from the introduced range will be less resistant to herbivory and grow faster than those from the home range; while the EICA will not be held for fast-growing genotypes, i.e., there will be no significant differences in growth and defense traits between the introduced and native fast-growing genotypes. We tested these predictions preliminarily using five populations of the invasive plant Alternanthera philoxeroides. This species has two varieties in its home range, which showed a distinct growth-defense strategy: the northern A. p. var. acutifolia (Apa) had higher growth rate but lower resistance, while the southern A. p. var. obtusifolia (Apo) had lower growth rate but higher resistance level. Our results suggest that the EICA hypothesis is consistent with the slow-growing Apo, but not with the fast-growing Apa. We suggest that evolutionary changes in growth or resistance following enemy release are influenced by variation in growth rate within an invasive alien plant. These findings have important implications for the EICA hypothesis, and may partially explain why previous studies have found evidence both for and against EICA.     

Competitive ability,not tolerance,may explain success of invasive plants over natives

When entering a new community, introduced species leave behind members of their native community while simultaneously forming novel biotic interactions. Escape from enemies during the process of introduction has long been hypothesized to drive the increased performance of invasive species. However, recent studies and quantitative syntheses find that invaders often receive similar, or even more, damage from enemies than do native species. Therefore, invasives may be those more tolerant to enemy damage, or those able to maintain competitive ability in light of enemy damage. Here, we investigate whether tolerance and competitive ability could contribute to invasive plant success. We determined whether invasive plants were more competitive than native or noninvasive exotic species in both the presence and absence of simulated herbivory. We found competition and herbivory additively reduced individual performance, and affected the performance of native, invasive, and noninvasive exotic species’ to the same degree. However, invasives exerted stronger competitive effects on an abundant native species (Elymus canadensis) in both the presence and absence of herbivory. Therefore, while invasive species responded similarly to competition and simulated herbivory, their competitive effects on natives may contribute to their success in their introduced range.     

Interactions between resource availability and enemy release in plant invasion

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

Increased chemical resistance explains low herbivore colonization of introduced seaweed

The success of introduced species is often attributed to release from co-evolved enemies in the new range and a subsequent decreased allocation to defense (EICA), but these hypotheses have rarely been evaluated for systems with low host-specificity of enemies. Here, we compare herbivore utilization of the brown seaweed, Fucus evanescens, and its coexisting competitors both in its native and new ranges, to test certain predictions derived from these hypotheses in a system dominated by generalist herbivores. While F. evanescens was shown to be a preferred host in its native range, invading populations supported a less diverse herbivore fauna and it was less preferred in laboratory choice experiments with important herbivores, when compared to co-occurring seaweeds. These results are consistent with the enemy release hypothesis, despite the fact that the herbivore communities in both regions were mainly composed of generalist species. However, in contrast to the prediction of EICA, analysis of anti-grazing compounds indicated a higher allocation to defense in introduced compared to native F. evanescens. The results suggest that the invader is subjected to less intense enemy control in the new range, but that this is due to an increased allocation to defense rather than release from specialized herbivores. This indicates that increased resistance to herbivory might be an important strategy for invasion success in systems dominated by generalist herbivores.     

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.     

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.     

Prevalence and evolutionary relationships of haematozoan parasites in native versus introduced populations of common myna Acridotheres tristis

The success of introduced species is frequently explained by their escape from natural enemies in the introduced region. We tested the enemy release hypothesis with respect to two well studied blood parasite genera (Plasmodium and Haemoproteus) in native and six introduced populations of the common myna Acridotheres tristis. Not all comparisons of introduced populations to the native population were consistent with expectations of the enemy release hypothesis. Native populations show greater overall parasite prevalence than introduced populations, but the lower prevalence in introduced populations is driven by low prevalence in two populations on oceanic islands (Fiji and Hawaii). When these are excluded, prevalence does not differ significantly. We found a similar number of parasite lineages in native populations compared to all introduced populations. Although there is some evidence that common mynas may have carried parasite lineages from native to introduced locations, and also that introduced populations may have become infected with novel parasite lineages, it may be difficult to differentiate between parasites that are native and introduced, because malarial parasite lineages often do not show regional or host specificity.     

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.     

Dispersal and spatial heterogeneity allow coexistence between enemies and protective mutualists

Protective mutualisms, where a symbiont reduces the negative effects of another species on a shared host, represent a common type of species interaction in natural communities, yet it is still unclear what ecological conditions might favor their emergence. Studies suggest that the initial evolution of protective mutualists might involve closely related pathogenic variants with similar life histories, but different competitive abilities and impacts on host fitness. We derive a model to evaluate this hypothesis and show that, in general, a protective variant cannot spread from rarity or exclude a more pathogenic strain. While the conditions allowing mutualist invasion are more likely with increased environmental productivity, they still depend on initial densities in the invaded patch exceeding a threshold, highlighting the likely importance of spatial structure and demographic stochasticity. Using a numerical simulation approach, we show that regional coexistence is in fact possible in an explicitly spatial system and that, under some circumstances, the mutualist population can exclude the enemy. More broadly, the establishment of protective mutualists may be favored when there are other life‐history differences from more pathogenic symbionts, such as vertical transmission or additional direct benefits to hosts.     

Enemy release at range edges: do invasive species escape their herbivores as they expand into new areas?

Aims We test the hypothesis that invasive plant species at their range edges experience lower herbivory and allocate less to defense at the edge of an expanding range edge than from more central parts of their distribution, during secondary invasion in a new range. Invasive plants are often able to spread rapidly through new areas. The success of invasive species in new ranges is frequently attributed to enemy release in these new areas and associated evolutionary changes minimizing allocation to defense in favor of growth and reproduction. Enemy release could also explain rapid advances of invasive species upon arriving in new habitats. If invasive species accumulate enemies over time in a new location, then these species may experience a release from their enemies at expanding range fronts. Enemy release at these range fronts may accelerate range expansion.Methods We used populations of four woody invasive species within the invaded range, and four native control species. We quantified leaf herbivory and leaf physical defense traits at both range central and range edge locations, over two 1-month sampling periods, sampled 7 months apart.Important findings Herbivory at the range edge did not differ to the range center but patterns were not consistent across species. There was a trend for lower herbivory at the range edge for Lantana camara, which was reflected in lower leaf toughness. Overall, leaf toughness was greater at the range edge location across invasive and control species. Physical defenses were different among range locations in a few species, though most species show the same trend, suggesting higher herbivory pressures at the range edge location or differences may be due to climatic factors. Leaves of L. camara were significantly less tough at range edges, suggesting that some species can potentially escape their enemies at range edges. However, our results overall do not support the hypothesis that plants at the edge of their ranges experience reduced impact from their enemies.     

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.     

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

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

Evolutionary origins and diversification of proteobacterial mutualists

Mutualistic bacteria infect most eukaryotic species in nearly every biome. Nonetheless, two dilemmas remain unresolved about bacterial–eukaryote mutualisms: how do mutualist phenotypes originate in bacterial lineages and to what degree do mutualists traits drive or hinder bacterial diversification? Here, we reconstructed the phylogeny of the hyperdiverse phylum Proteobacteria to investigate the origins and evolutionary diversification of mutualistic bacterial phenotypes. Our ancestral state reconstructions (ASRs) inferred a range of 34–39 independent origins of mutualist phenotypes in Proteobacteria, revealing the surprising frequency with which host-beneficial traits have evolved in this phylum. We found proteobacterial mutualists to be more often derived from parasitic than from free-living ancestors, consistent with the untested paradigm that bacterial mutualists most often evolve from pathogens. Strikingly, we inferred that mutualists exhibit a negative net diversification rate (speciation minus extinction), which suggests that mutualism evolves primarily via transitions from other states rather than diversification within mutualist taxa. Moreover, our ASRs infer that proteobacterial mutualist lineages exhibit a paucity of reversals to parasitism or to free-living status. This evolutionary conservatism of mutualism is contrary to long-standing theory, which predicts that selection should often favour mutants in microbial mutualist populations that exploit or abandon more slowly evolving eukaryotic hosts.