Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia

One of the influential hypotheses invoked to explain why species become invasive following introduction is that release from natural enemies favours a shift in investment from defence to traits enhancing growth and reproduction. Silene latifolia was introduced from Europe (EU) to North America (NA) c. 200 years ago where it experiences lower damage by natural enemies. A common garden experiment in EU using seeds from 20 EU and 20 NA populations revealed (1) genetically‐based differences in life history between plants from EU and NA; plants from NA have evolved a weedy phenotype that flowers earlier, and has a two‐ to threefold higher reproductive potential; (2) higher susceptibility of NA plants to fungal infection, fruit predation, and aphid infestation. These results suggest that the invasive NA phenotype has evolved at the expense of defensive abilities. Despite this increased susceptibility to enemies, NA populations still outperformed EU populations in this common garden.     

The effect of inbreeding on defence against multiple enemies in Datura stramonium

The ability of plants to respond to natural enemies might depend on the availability of genetic variation for the optimal phenotypic expression of defence. Selfing can affect the distribution of genetic variability of plant fitness, resistance and tolerance to herbivores and pathogens. The hypothesis of inbreeding depression influencing plant defence predicts that inbreeding would reduce resistance and tolerance to damage by natural enemies relative to outcrossing. In a field experiment entailing experimentally produced inbred and outcrossed progenies, we assessed the effects of one generation of selfing on Datura stramonium resistance and tolerance to three types of natural enemies, herbivores, weevils and a virus. We also examined the effect of damage on relative growth rate (RGR), flower, fruit, and seed production in inbred and outcrossed plants. Inbreeding significantly reduced plant defence to natural enemies with an increase of 4% in herbivore damage and 8% in viral infection. These results indicate inbreeding depression in total resistance. Herbivory increased 10% inbreeding depression in seed number, but viral damage caused inbred and outcrossed plants to have similar seed production. Inbreeding and outcrossing effects on fitness components were highly variable among families, implying that different types or numbers of recessive deleterious alleles segregate following inbreeding in D. stramonium. Although inbreeding did not equally alter all the interactions, our findings indicate that inbreeding reduced plant defence to herbivores and pathogens in D. stramonium.     

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.     

Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction

Successful plant invasions are often attributed to increased plant size, reproduction, or release from natural enemies, but the generality and persistence of these patterns remains widely debated. Meta-analysis was used to quantitatively assess invasive plant performance and release from enemy damage and how these change with residence time and geographic distribution. Invasive plants were compared either in their introduced and home ranges or with native congeners in the introduced range. Invasive plants in the introduced range were generally larger, allocated more to reproduction, and had lower levels of herbivore damage compared with conspecifics in the home range; pathogen attack, however, varied widely. In congener comparisons, invasive and native plants did not differ in size or herbivory, but invaders did allocate less to reproduction and had lower levels of pathogen damage. Time since introduction was a significant nonlinear predictor of enemy release for both herbivores and pathogens, with initial release in recently arrived species and little to no release after 50 to 200 years. Geographic distribution was also a significant nonlinear predictor of enemy release. The observed nonlinear relationships are consistent with dynamic invasions and may define targets for eradication efforts if these patterns hold up for individual species.     

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.     

Tetranychus evansi spider mite populations suppress tomato defenses to varying degrees

Plant defense suppression is an offensive strategy of herbivores, in which they manipulate plant physiological processes to increase their performance. Paradoxically, defense suppression does not always benefit the defense‐suppressing herbivores, because lowered plant defenses can also enhance the performance of competing herbivores and can expose herbivores to increased predation. Suppression of plant defense may therefore entail considerable ecological costs depending on the presence of competitors and natural enemies in a community. Hence, we hypothesize that the optimal magnitude of suppression differs among locations. To investigate this, we studied defense suppression across populations of Tetranychus evansi spider mites, a herbivore from South America that is an invasive pest of solanaceous plants including cultivated tomato, Solanum lycopersicum, in other parts of the world. We measured the level of expression of defense marker genes in tomato plants after infestation with mites from eleven different T. evansi populations. These populations were chosen across a range of native (South American) and non‐native (other continents) environments and from different host plant species. We found significant variation at three out of four defense marker genes, demonstrating that T. evansi populations suppress jasmonic acid‐ and salicylic acid‐dependent plant signaling pathways to varying degrees. While we found no indication that this variation in defense suppression was explained by differences in host plant species, invasive populations tended to suppress plant defense to a smaller extent than native populations. This may reflect either the genetic lineage of T. evansi—as all invasive populations we studied belong to one linage and both native populations to another—or the absence of specialized natural enemies in invasive T. evansi populations.     

Selection on tropane alkaloids in native and non‐native populations of Datura stramonium

Theories of plant invasion based on enemy release in a new range assume that selection exerted by specialist herbivores on defence traits should be reduced, absent, or even selected against in the new environment. Here, we measured phenotypic selection on atropine and scopolamine concentration of Datura stramonium in eight native (Mexico) and 14 non‐native (Spain) populations. Native populations produced between 20 and 40 times more alkaloid than non‐native populations (atropine: 2.0171 vs. 0.0458 mg/g; scopolamine: 1.004 vs. 0.0488 mg/g, respectively). Selection on alkaloids was negative for atropine and positive for scopolamine concentration in both ranges. However, the effect sizes of selection gradients were only significant in the native range. Our results support the assumption that the reduction of plant defence in the absence of the plant's natural enemies in invasive ranges is driven by natural selection.     

Comparison of invertebrate herbivores on native and non‐native Senecio species: Implications for the enemy release hypothesis

The enemy release hypothesis posits that non‐native plant species may gain a competitive advantage over their native counterparts because they are liberated from co‐evolved natural enemies from their native area. The phylogenetic relationship between a non‐native plant and the native community may be important for understanding the success of some non‐native plants, because host switching by insect herbivores is more likely to occur between closely related species. We tested the enemy release hypothesis by comparing leaf damage and herbivorous insect assemblages on the invasive species Senecio madagascariensis Poir. to that on nine congeneric species, of which five are native to the study area, and four are non‐native but considered non‐invasive. Non‐native species had less leaf damage than natives overall, but we found no significant differences in the abundance, richness and Shannon diversity of herbivores between native and non‐native Senecio L. species. The herbivore assemblage and percentage abundance of herbivore guilds differed among all Senecio species, but patterns were not related to whether the species was native or not. Species‐level differences indicate that S. madagascariensis may have a greater proportion of generalist insect damage (represented by phytophagous leaf chewers) than the other Senecio species. Within a plant genus, escape from natural enemies may not be a sufficient explanation for why some non‐native species become more invasive than others.     

Non-native Microstegium vimineum populations collapse with fungal leaf spot disease outbreak

Non-native plants may meet little resistance in the novel range if they leave their biological enemies at home. As a result, species invasion can be rapid and appear unlimited. However, with time, organisms may acquire novel enemies in the novel range, or home-range enemies also may colonize the novel range. For plants, several authors have suggested that enemy release may give way to enemy acquisition in which pathogens accumulate and suppresses non-native plants. The ‘naturalization’ that occurs with acquired enemies may take decades to develop, yet most species invasion research lasts less than 4 years, and data tracking plant invasion before and after the appearance of pathogens are rare. Microstegium vimineum is an Asian grass that has invaded deciduous forest habitats in the southern Midwestern and Southeastern USA and is currently expanding in the Northeastern USA. We recorded widespread expansions in M. populations in North Carolina and Georgia (USA) between 2009 and 2011 but noticed that a fungal pathogen (indicated by leaf lesions; Bipolaris sp.) appeared on several of the populations in 2011. In 2019, we re-sampled these populations to determine whether the appearance of the fungal pathogen corresponded with a suppression of M. vimineum expansion. We found the once-expanding M. vimineum populations in retreat in 2019, and the plant population contractions were greater (and seed production lesser) where the fungal leaf spot disease was most extensive. These results suggest that enemy acquisition suppressed an active non-native plant invasion. We also found that where M. vimineum populations declined (or disappeared) native plants appeared to fill in the gap. Hence, whereby exotic species may gain advantage in novel habitat with the loss of their native-range pathogens, with longer time spans, enemy release may give way to enemy acquisition and native populations may recover if they are immune to the pathogens.

     

Relatively weak inbreeding depression in selfing but also in outcrossing populations of North American Arabidopsis lyrata

Hermaphroditic plants can potentially self‐fertilize, but most possess adaptations that promote outcrossing. However, evolutionary transitions to higher selfing rates are frequent. Selfing comes with a transmission advantage over outcrossing, but self‐progeny may suffer from inbreeding depression, which forms the main barrier to the evolution of higher selfing rates. Here, we assessed inbreeding depression in the North American herb Arabidopsis lyrata, which is normally self‐incompatible, with a low frequency of self‐compatible plants. However, a few populations have become fixed for self‐compatibility and have high selfing rates. Under greenhouse conditions, we estimated mean inbreeding depression per seed (based on cumulative vegetative performance calculated as the product of germination, survival and aboveground biomass) to be 0.34 for six outcrossing populations, and 0.26 for five selfing populations. Exposing plants to drought and inducing defences with jasmonic acid did not magnify these estimates. For outcrossing populations, however, inbreeding depression per seed may underestimate true levels of inbreeding depression, because self‐incompatible plants showed strong reductions in seed set after (enforced) selfing. Inbreeding‐depression estimates incorporating seed set averaged 0.63 for outcrossing populations (compared to 0.30 for selfing populations). However, this is likely an overestimate because exposing plants to 5% CO₂ to circumvent self‐incompatibility to produce selfed seed might leave residual effects of self‐incompatibility that contribute to reduced seed set. Nevertheless, our estimates of inbreeding depression were clearly lower than previous estimates based on the same performance traits in outcrossing European populations of A. lyrata, which may help explain why selfing could evolve in North American A. lyrata.     

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

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

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.     

Adaptive and non‐adaptive evolution of trait means and genetic trait correlations for herbivory resistance and performance in an invasive plant

The EICA‐hypothesis predicts that invading plants adapt to their novel environment by evolving increased performance and reduced resistance in response to the release from natural enemies, and assumes a resource allocation tradeoff among both trait groups as mechanistic basis of this evolutionary change. Using the plant Silene latifolia as a study system, we tested these predictions by investigating whether 1) invasive populations evolved lower resistance and higher performance, 2) this evolutionary change is indeed adaptive, and 3) there is a negative genetic correlation between performance and resistance (i.e. a tradeoff) in native and introduced individuals. Moreover, we sampled eight native and eight invasive populations and determined their population co‐ancestry based on neutral SSR‐markers. We performed controlled crossings to produce five sib‐groups per population and exposed them to increased and reduced levels of enemy attack in a full‐factorial experiment to estimate performance and resistance. With these data, we performed trait‐by‐trait comparisons between ranges with ‘animal models’ that account for population co‐ancestry to quantify the amount of variance in traits explained by non‐adaptive versus adaptive evolution. Moreover, we tested for genetic correlations among performance and resistance traits within sib‐groups. We found significant reductions in resistance and increases in performance in invasive versus native populations, which could largely be attributed to adaptive evolution. While we detected a non‐significant trend towards negative genetic performance × resistance correlations in native populations, invasive populations exhibited both significant and non‐significant positive correlations. In summary, these results do not support a shift of performance and resistance trait values along a tradeoff line in response to enemy release, as predicted by EICA. They rather suggest that the independent evolution of both traits is not constrained by a tradeoff, and that various selective agents (including resource availability) interact in shaping both traits and in weakening negative genetic correlations in the invaded habitat.     

The invasive shrub Buddleja davidii performs better in its introduced range

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

Geographic patterns of herbivory and resource allocation to defense, growth, and reproduction in an invasive biennial, Alliaria petiolata

We investigated geographic patterns of herbivory and resource allocation to defense, growth, and reproduction in an invasive biennial, Alliaria petiolata, to test the hypothesis that escape from herbivory in invasive species permits enhanced growth and lower production of defensive chemicals. We quantified herbivore damage, concentrations of sinigrin, and growth and reproduction inside and outside herbivore exclusion treatments, in field populations in the native and invasive ranges. As predicted, unmanipulated plants in the native range (Hungary, Europe) experienced greater herbivore damage than plants in the introduced range (Massachusetts and Connecticut, USA), providing evidence for enemy release, particularly in the first year of growth. Nevertheless, European populations had consistently larger individuals than US populations (rosettes were, for example, eightfold larger) and also had greater reproductive output, but US plants produced larger seeds at a given plant height. Moreover, flowering plants showed significant differences in concentrations of sinigrin in the invasive versus native range, although the direction of the difference was variable, suggesting the influence of environmental effects. Overall, we observed less herbivory, but not increased growth or decreased defense in the invasive range. Geographical differences in performance and leaf chemistry appear to be due to variation in the environment, which could have masked evolved differences in allocation.     

Rapid evolution of Medicago polymorpha during invasion shifts interactions with the soybean looper

The Enemy Release Hypothesis posits that invasion of novel habitats can be facilitated by the absence of coevolved herbivores. However, a new environment and interactions with unfamiliar herbivores may impose selection on invading plants for traits that reduce their attractiveness to herbivores or for enhanced defenses compared to native host plants, leading to a pattern similar to enemy release but driven by evolutionary change rather than ecological differences. The Shifting Defense Hypothesis posits that plants in novel habitats will shift from specialized defense mechanisms to defense mechanisms effective against generalist herbivores in the new range. We tested these ideas by comparing herbivore preference and performance of native (Eurasia)‐ and invasive (New World)‐range Medicago polymorpha, using a generalist herbivore, the soybean looper, that co‐occurs with M. polymorpha in its New World invaded range. We found that soybean loopers varied in preference and performance depending on host genotype and that overall the herbivore preferred to consume plant genotypes from naïve populations from Eurasia. This potentially suggests that range expansion of M. polymorpha into the New World has led to rapid evolution of a variety of traits that have helped multiple populations become established, including those that may allow invasive populations to resist herbivory. Thus, enemy release in a novel range can occur through rapid evolution by the plant during invasion, as predicted by the Shifting Defense Hypothesis, rather than via historical divergence.     

Climate warming affects biological invasions by shifting interactions of plants and herbivores

Plants and herbivorous insects can each be dramatically affected by temperature. Climate warming may impact plant invasion success directly but also indirectly through changes in their natural enemies. To date, however, there are no tests of how climate warming shifts the interactions among invasive plants and their natural enemies to affect invasion success. Field surveys covering the full latitudinal range of invasive Alternanthera philoxeroides in China showed that a beetle introduced for biocontrol was rare or absent at higher latitudes. In contrast, plant cover and mass increased with latitude. In a 2‐year field experiment near the northern limit of beetle distribution, we found the beetle sustained populations across years under elevated temperature, dramatically decreasing A. philoxeroides growth, but it failed to overwinter in ambient temperature. Together, these results suggest that warming will allow the natural enemy to expand its range, potentially benefiting biocontrol in regions that are currently too cold for the natural enemy. However, the invader may also expand its range further north in response to warming. In such cases where plants tolerate cold better than their natural enemies, the geographical gap between plant and herbivorous insect ranges may not disappear but will shift to higher latitudes, leading to a new zone of enemy release. Therefore, warming will not only affect plant invasions directly but also drive either enemy release or increase that will result in contrasting effects on invasive plants. The findings are also critical for future management of invasive species under climate change.     

No inbreeding depression in laboratory‐reared individuals of the parasitoid wasp Allotropa burrelli

Inbreeding depression is a major concern in almost all human activities relating to plant and animal breeding. The biological control of pests with natural enemies is no exception, because populations of biocontrol agents experience a series of bottlenecks during importation, rearing, and introduction. A classical biological control program for the Comstock mealybug Pseudococcus comstocki (Hemiptera: Pseudococcidae) was initiated in France in 2008, based on the introduction of an exotic parasitoid, Allotropa burrelli Mues. (Hymenoptera: Platygastridae), a haplodiploid parasitoid imported from Japan. We evaluated the sensitivity of A. burrelli to inbreeding, to optimize rearing and release strategies. We compared several morphological and life‐history traits between the offspring of siblings and the offspring of unrelated parents. We took into account the low level of genetic variability due to the relatively small size of laboratory‐reared populations by contrasting two types of pedigree: one for individuals from a strain founded from a single field population, and the other generated by hybridizing individuals from two strains founded from two highly differentiated populations. Despite this careful design, we obtained no evidence for a negative impact of inbreeding on laboratory‐reared A. burrelli. We discussed the results in light of haplodiploid sex determination and parasitoid mating systems, and classical biological control practices.     

History of exposure to herbivores increases the compensatory ability of an invasive plant

Release from natural enemies is frequently cited as an important factor contributing to plant invasions. But such effects are likely to be temporary—native herbivores can form new plant-herbivore associations and co-evolved insects might reach the new range. While the potential effects of the initial enemy release have been well studied, the consequences of any resumption of herbivory are poorly understood. Alternanthera philoxeroides is one of the most widespread invasive plants in China and is attacked both by a specialist herbivore introduced from the native range, Agasicles hygrophila, and a native beetle Cassida piperata Hope which has formed a new association. However, these insects are not found throughout the invaded range. To test the effect of the history of population exposure to herbivory on compensatory ability, plants were cultured from 14 populations around China that differed in whether A. hygrophila or C. piperata were present. Treatment plants were exposed to herbivory by A. hygrophila for a week until 50% of the leaf area was defoliated, then grown for 80 days. Plants from populations with prior exposure to herbivory (of any kind) accumulated more root mass than populations without prior exposure, indicating that prior exposure to insects can stimulate plant compensation to herbivory. We would recommend that potential changes in plant tolerance in response to prior exposure to herbivory are considered in invasive plant management plans that employ bio-control agents.     

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

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