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.     

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.     

Invasive parasites are detectable by their abundance-occupancy relationships: the case of helminths from Liza haematocheilus (Teleostei: Mugilidae)

The biogeographic patterns of abundance and prevalence of helminths from Liza haematocheilus were studied across its native (Sea of Japan) and introduced (Sea of Azov) distribution ranges. Abundance-occupancy relationships (AORs) were tested for the core-satellite and enemy release (ERH) species hypotheses in eight and 14 host samples from the native and introduced host ranges, respectively. The AOR model fitted parasite data extremely well, irrespective of whether the host or the parasite species were native or invasive. Except for co-introduced monogeneans, species were less abundant and prevalent in the introduced host population than in the native one, which agrees well with the ERH. Two occupancy patterns were observed. A unimodal, right-skewed distribution of prevalence frequency was common for the acquired groups of helminth parasites in the introduced range, whereas a bimodal distribution was more common in the native range. Core species in the native range were monogeneans, adult and larval digeneans, whereas host-specific, co-introduced monogeneans were the only core species in the introduced range. Acquired grey-mullet specialists and host generalists infected only a small portion of the introduced host population with low mean abundance. These results indicate that strict host specificity, together with a direct life cycle, are the traits that enabled helminth species to entirely occupy the invasive host population. The AORs showed that parasite individuals tend to accumulate in a relatively small fraction of susceptible introduced hosts, probably as an adaptation to enhance mating opportunities, thereby providing a mechanistic explanation of the ERH. All this evidence suggests that co-introduced and acquired species use the introduced host population in very different ways. Therefore, we posit that the examination of AORs can be instrumental in understanding the role of co-introduced parasites in invasion theory.     

Specificity of extrafloral nectar induction by herbivores differs among native and invasive populations of tallow tree

Background and Aims

Invasive plants can be released from specialist herbivores and encounter novel generalists in their introduced ranges, leading to variation in defence among native and invasive populations. However, few studies have examined how constitutive and induced indirect defences change during plant invasion, especially during the juvenile stage.

Methods

Constitutive extrafloral nectar (EFN) production of native and invasive populations of juvenile tallow tree (Triadica sebifera) were compared, and leaf clipping, and damage by a native specialist (Noctuid) and two native generalist caterpillars (Noctuid and Limacodid) were used to examine inducible EFN production.

Key results

Plants from introduced populations had more leaves producing constitutive EFN than did native populations, but the content of soluble solids of EFN did not differ. Herbivores induced EFN production more than simulated herbivory. The specialist (Noctuid) induced more EFN than either generalist for native populations. The content of soluble solids in EFN was higher (2·1 times), with the specialist vs. the generalists causing the stronger response for native populations, but the specialist response was always comparable with the generalist responses for invasive populations.

Conclusions

These results suggest that constitutive and induced indirect defences are retained in juvenile plants of invasive populations even during plant establishment, perhaps due to generalist herbivory in the introduced range. However, responses specific to a specialist herbivore may be reduced in the introduced range where specialists are absent. This decreased defence may benefit specialist insects that are introduced for classical biological control of invasive plants.     

Does enemy release matter for invasive plants? evidence from a comparison of insect herbivore damage among invasive,non-invasive and native congeners

One of the most popular single-factor hypotheses that have been proposed to explain the naturalization and spread of introduced species is the enemy release hypothesis (ERH). One ramification of the ERH is that invasive plants sustain less herbivore damage than their native counterparts in the invaded range. However, introduced plants, invasive or not, may experience less herbivore damage than the natives. Therefore, to test the role of natural enemies in the success of invasive plants, studies should include both invasive as well as non-invasive introduced species. In this study, we employed a novel three-way comparison, in which we compared herbivore damage among native, introduced invasive, and introduced non-invasive Eugenia (Myrtaceae) in South Florida. We found that introduced Eugenia, both invasive and non-invasive, sustained less herbivore damage, especially damage by oligophagous and endophagous insects, than native Eugenia. However, the difference in insect damage between introduced invasive and introduced non-invasive Eugenia was not significant. Escape from herbivores may not account for the spread of invasive Eugenia. We would not have been able to draw this conclusion without inclusion of the non-invasive Eugenia species in the study.     

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.     

Top-down pressure by generalist and specialist natural enemies in relation to habitat heterogeneity and resource availability

Habitat heterogeneity might promote the abundance and richness of natural enemies potentially leading to higher top-down pressure on herbivorous insects. Heterogeneous habitats could provide natural enemies with more abundant and alternative resources and a greater variety of micro-habitats. Natural enemies with different searching behaviours, e.g. generalists and specialists, could be affected in different ways by habitat heterogeneity, thus affecting their pressure on herbivorous insects.To understand how top-down pressure on herbivorous insects is promoted by habitat heterogeneity, it is crucial to investigate which parameters contributing to habitat heterogeneity affect not only the abundance and richness but also the searching behaviour of different natural enemies. We investigated the relationship between heterogeneity in forest habitats and the top-down pressure exerted by generalist predators and specialist parasitoids on larvae of the European pine sawfly (Neodiprion sertifer).We used forest stands with endemic or epidemic densities of resident sawfly populations. Within each stand we selected experimental trees to create variation in tree species diversity and density in their surrounding area, i.e. habitat heterogeneity. We found that a higher tree density increased the predation by generalists on sawfly larvae in stands with endemic sawfly densities. Parasitoids were less successful in stands with endemic sawfly densities. Total mortality depended on stand character and the proportion of pine around experimental trees.The explained variation in the response variables by the models is relatively low, indicating that other measures of heterogeneity, like understory vegetation and presence of dead wood could contribute to the observed variation. Also, interference between generalist and specialist enemies could affect the realized mortality pressure. Thus, the effect of tree species diversity in combination with these other measures of heterogeneity needs to be recognized to promote the presence and the activity of natural enemies in managed habitats.     

Native or nonnative host plants: What is better for a specialist moth?

The enemy release hypothesis (ERH) predicts that the lack of natural enemies, such as herbivores, contributes to the success of nonnative plants as colonizers. Larvae of the Neotropical specialist moth Utetheisa ornatrix (Erebidae: Arctiinae) can feed on unripe seeds and leaves of both native and nonnative Crotalaria species (Fabaceae). Despite some species being able to eat nonnative plants, such behavior can impair the herbivore, as they are not adapted to the alien plant, and still contribute to the success of the nonnative species via enemy release. We tested the performance of the moth from hatching to adulthood fed on two native (C. micans and C. paulina) and two nonnative (C. pallida, C. juncea) host plants. Utetheisa ornatrix performed better (lower development time, heavier pupae and more eggs) on the native host plants than in the nonnative. However, larva performance in nonnative C. pallida was similar to that in the native host plants. Using the larval weight 7 days after hatching from the eggs as a proxy for performance in twelve Crotalaria species (five Neotropical natives, four nonnatives from Afrotropical region, and three nonnatives from India), we found similar results. Crotalaria nutritional compounds, the defensive pyrrolizidine alkaloids and Crotalaria phylogeny did not explain moth performance. Our results give some support to the ERH. The good moth performance in nonnative C. pallida may be related to its high availability as host plant for U. ornatrix, and its longer time since their introduction in Neotropics which would provide opportunity for the moth to adapt.     

Differences in physiological traits and resistances of <Emphasis Type="Italic">Alternanthera philoxeroides</Emphasis> after herbivory by generalists and specialists

Many researchers have surveyed damages caused by natural enemies of invasive plants in both native and introduced ranges to test the enemy release hypothesis. In this study, we report our findings on the physiological and morphological impacts of a co-evolved specialist insect (Agasicles hygrophila) and two generalist insects (Atractomorpha sinensis and Hymenia recurvalis) in introduced ranges on an invasive plant, Alternanthera philoxeroides, in both field trials and controlled environments. The resistance of A. philoxeroides against the generalists and the specialist was also studied. We obtained consistent results in both the field trials and the controlled treatments: both the generalists and the specialist decreased leaf biomass, photosynthesis, leaf nitrogen content, and total leaf non-structural carbohydrate content in A. philoxeroides. However, the specialist decreased leaf mass, photosynthesis, and leaf nitrogen content more acutely than the generalists. Moreover, A. philoxeroides increased both leaf lignin and cellulose concentrations upon the generalists’ attack but only increased cellulose concentration in response to the specialist. Our results showed that even under the same population density, the co-evolved specialists from original ranges caused more severe morphological and physiological damage to A. philoxeroides than the generalists in introduced ranges. This revealed that invasive plants released some herbivory stress before their co-evolved specialists were introduced, which may contribute to the superior performance of invasive plants in introduced regions.     

Plant secondary substances and insects behaviour

Allelochemicals are storing in different location in plant tissues as inactive form. Number of identified compounds may now exceed 100,000. Environmental factors have an effect on allelochemicals concentration in plants. Many allelochemicals classified as toxins or deterrents for herbivorous insects. Allelochemicals play a major role in feeding or ovipositing stimulants for some specialist insects. Consumption and assimilation of herbivorous insects had affected by the type of allelochemicals in host plants. Allelochemicals have an acute or chronic toxicity on herbivorous insects. Most specialist herbivorous insects rely heavily of ingested plant allelochemicals. Plant allelochemicals may influence an insect's susceptibility to pathogens such as bacteria, fungi and nematode. Specialists herbivorous insect can be using the allelochemicals in their host plants as protection against natural enemies. Some herbivorous insects are synthesising the aggregation, attracting, alarm or mating pheromone from the allelochemicals in their host plants.     

Realized vs apparent reduction in enemies of the European starling

Release from parasites, pathogens or predators (i.e. enemies) is a widely cited ‘rule of thumb’ to explain the proliferation of nonindigenous species in their introduced regions (i.e. the ‘enemy release hypothesis’, or ERH). Indeed, profound effects of some parasites and predators on host populations are well documented. However, some support for the ERH comes from studies that find a reduction in the species richness of enemies in the introduced range, relative to the native range, of particular hosts. For example, data on helminth parasites of the European starling in both its native Eurasia and in North America support a reduction of parasites in the latter. However, North American ‘founder’ starlings were likely not chosen randomly from across Eurasia. This could result in an overestimation of enemy release since enemies affect their hosts on a population level. We control for the effects of subsampling colonists and find, contrary to previous reports, no evidence that introduced populations of starlings experienced a reduction in the species richness of helminth parasites after colonization of North America. These results highlight the importance of choosing appropriate contrast groups in biogeographical analyses of biological invasions to minimize the confounding effects of ‘propagule biases’.     

Differences in herbivore damage and performance among <Emphasis Type="Italic">Arctium minus</Emphasis> (burdock) genotypes sampled from a geographic gradient: a common garden experiment

Performance of plant species does not necessarily decline as they approach their geographic range limits. One reason for this may be a loss of natural enemies in marginal populations. Such patterns have been found in native species, but also may occur for exotics if they have not already escaped their herbivores in invaded regions. For instance, the Eurasian biennial Arctium minus (common burdock) is attacked by a variety of native and introduced insects in its new North American range. Previously, research has shown that damage by these herbivores strongly decreases towards the northern range limit of this species. This gradient might reflect a genetic cline in resistance to herbivores, or geographic variation in herbivore abundance. To distinguish between these possibilities, herbivore damage to leaves and seeds of A. minus was measured in a common garden experiment with genotypes sampled from 11 populations along a 550 km transect extending from southern Ontario towards burdock’s northern range limit. As well, a freezing tolerance experiment was performed with the important lepidopteran seed predator Metzneria lappella, and palatability experiments were performed with two generalists, the snail Cepaea nemoralis and the moth Trichoplusia ni. Although there were some differences in damage among populations, results indicated that latitudinal differences in herbivore damage are not explained by genotypic differences among populations, but instead are likely to result from the absence of herbivores from colder sites. Escape of A. minus from its usual herbivores may increase performance of marginal populations, and contribute to future spread.     

Unifying concepts and mechanisms in the specificity of plant-enemy interactions

Host ranges are commonly quantified to classify herbivores and plant pathogens as either generalists or specialists. Here, we summarize patterns and mechanisms in the interactions of plants with these enemies along different axes of specificity. We highlight the many dimensions within which plant enemies can specify and consider the underlying ecological, evolutionary and molecular mechanisms. Host resistance traits and enemy effectors emerge as central players determining host utilization and thus host range. Finally, we review approaches to studying the causes and consequences of variation in the specificity of plant-enemy interactions. Knowledge of the molecular mechanisms that determine host range is required to understand host shifts, and evolutionary transitions among specialist and generalist strategies, and to predict potential host ranges of pathogens and herbivores.     

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.     

Ants visiting extrafloral nectaries and pyrrolizidine alkaloids may shape how a specialist herbivore feeds on its host plants

The presence of extrafloral nectaries (EFNs) attracts predators and parasitoids, and protects the plant against herbivorous insects. By improving plant defences, EFNs reduce the fitness of herbivores. The use of similar host plants with no EFNs or adaptations in response to predators and parasitoids may enhance herbivore fitness. In this context, we studied the feeding habit (on leaves or on unripe seeds inside the pods) of larvae of the specialist moth Utetheisa ornatrix in two Crotalaria host plant species in which EFNs are present (C. micans) or absent (C. paulina). We hypothesized that the moths’ feeding habit was influenced by its natural enemies via their presence on EFNs. In C. micans, we found more larvae feeding inside the pods rather than on the leaves, while in C. paulina, larvae were found in both parts of the plant. There was greater activity of natural enemies in C. micans than in C. paulina. The moth sequesters enough pyrrolizidine alkaloid (PAs) to defend against predators in the leaves and seeds of C. paulina, but only in seeds of C. micans. Therefore, a change in the feeding habit in U. ornatrix larvae is a plastic response that depends on whether EFNs are present or not, or whether PA concentrations are low or high. This change does not affect overall moth performance. However, other factors, such as pod hardness, predation by organisms other than those visiting EFNs or even parasitoids cannot be ruled out as being responsible for the change in feeding habit. To date, both the EFNs and PAs in Crotalaria species are a parsimonious explanation of how larvae of U. ornatrix use different species of Crotalaria for feeding.     

Trade-offs in responses to host plants within a population of a generalist herbivore,Christoneura rosaceana

Evolutionary constraints on the ability of herbivores to efficiently use a set of phytochemically similar hosts, while maintaining a high performance on phytochemically different hosts, are central in explaining the predominance of host specialization in phytophagous insects. Such feeding trade-offs could be manifested within insect populations as negative genetic correlations in fitness on different host species. We tested the hypothesis that feeding trade-offs were present within a population of the obliquebanded leafroller,Choristoneura rosaceana (Harris). Components of fitness were measured in families originating from an apple orchard that were fed on four host-plant species in the laboratory. Under the conditions of this experiment, all across-host genetic correlations were strongly positive, suggesting that this population comprised true generalists. With the exception of diapausing propensity, the heritability of the fitness components tended to be lower in caterpillars fed on apple leaves than in insects fed other hosts. This suggests a constraint on the selective response of the fitness components in the orchard environment.     

Resistance to Plant Invasion? A Native Specialist Herbivore Shows Preference for and Higher Fitness on an Introduced Host

The response of native herbivores to the introduction of a new plant to the community has important implications for plant invasion. Under the Enemy Release Hypothesis introduced species become invasive because of reduced enemy control in the new range, while under the New Association Hypothesis introduced species lack effective defenses against native enemies because they do not share an evolutionary history. I tested the response of a native South-American specialist herbivore Utetheisa ornatrix (Lepidoptera: Arctiidae) to a native (Crotalaria incana) and an introduced host (Crotalaria pallida) (Fabaceae: Papilionoideae). I compared seed predation rates between the two hosts in the field, and I tested preference and performance traits with common garden experiments. Utetheisa ornatrix caused much higher seed predation rates on the introduced host than on the native host. Females also preferred to oviposit on the introduced over the native host. Additionally, larvae feeding on the introduced host had higher fitness (higher pupal weight) than larvae feeding on the native host. I discuss how the response of this specialist herbivore to this introduced host plant contradicts the predictions of the Enemy Release Hypothesis and support the New Association Hypothesis. This study shows that the New Association Hypothesis can also be true for specialist herbivores.     

Comparative analysis of quantitative trait loci controlling glucosinolates,myrosinase and insect resistance in Arabidopsis thaliana

Evolutionary interactions among insect herbivores and plant chemical defenses have generated systems where plant compounds have opposing fitness consequences for host plants, depending on attack by various insect herbivores. This interplay complicates understanding of fitness costs and benefits of plant chemical defenses. We are studying the role of the glucosinolate-myrosinase chemical defense system in protecting Arabidopsis thaliana from specialist and generalist insect herbivory. We used two Arabidopsis recombinant inbred populations in which we had previously mapped QTL controlling variation in the glucosinolate-myrosinase system. In this study we mapped QTL controlling resistance to specialist (Plutella xylostella) and generalist (Trichoplusia ni) herbivores. We identified a number of QTL that are specific to one herbivore or the other, as well as a single QTL that controls resistance to both insects. Comparison of QTL for herbivory, glucosinolates, and myrosinase showed that T. ni herbivory is strongly deterred by higher glucosinolate levels, faster breakdown rates, and specific chemical structures. In contrast, P. xylostella herbivory is uncorrelated with variation in the glucosinolate-myrosinase system. This agrees with evolutionary theory stating that specialist insects may overcome host plant chemical defenses, whereas generalists will be sensitive to these same defenses.     

Influence of insects and fungal pathogens on individual and population parameters of <Emphasis Type="Italic">Cirsium arvense</Emphasis> in its native and introduced ranges

Introduced weeds are hypothesized to be invasive in their exotic ranges due to release from natural enemies. Cirsium arvense (Californian, Canada, or creeping thistle) is a weed of Eurasian origin that was inadvertently introduced to New Zealand (NZ), where it is presently one of the worst invasive weeds. We tested the ‘enemy release hypothesis’ (ERH) by establishing natural enemy exclusion plots in both the native (Europe) and introduced (NZ) ranges of C. arvense. We followed the development and fate of individually labelled shoots and recorded recruitment of new shoots into the population over two years. Natural enemy exclusion had minimal impact on shoot height and relative growth rate in either range. However, natural enemies did have a significant effect on shoot population growth and development in the native range, supporting the ERH. In year one, exclusion of insect herbivores increased mean population growth by 2.1–3.6 shoots m⁻², and in year two exclusion of pathogens increased mean population growth by 2.7–4.1 shoots m⁻². Exclusion of insect herbivores in the native range also increased the probability of shoots developing from the budding to the reproductive growth stage by 4.0× in the first year, and 13.4× in the second year; but exclusion of pathogens had no effect on shoot development in either year. In accordance with the ERH, exclusion of insect herbivores and pathogens did not benefit shoot development or population growth in the introduced range. In either range, we found no evidence for an additive benefit of dual exclusion of insects and pathogens, and in no case was there an interaction between insect and pathogen exclusion. This study further demonstrates the value of conducting manipulative experiments in the native and introduced ranges of an invasive plant to elucidate invasion mechanisms.     

Decreased resistance and increased tolerance to native herbivores of the invasive plant Sapium sebiferum

Release from natural enemies may favor invasive plants evolving traits associated with reduced herbivore‐resistance and faster‐growth in introduced ranges. Given a genetic trade‐off between resistance and tolerance, invasive plants could also become more tolerant to herbivory than conspecifics in the native range. We conducted a field common garden study in the native range of Sapium sebiferum using seeds from native Chinese populations and invasive North American populations to compare their growth and herbivory resistance. We also performed a cage‐pot experiment to compare their resistance and tolerance to Bikasha collaris beetles that are specialist feeders on S. sebiferum trees in China. Results of the common garden study showed that Sapium seedlings of invasive populations relative to native populations were more frequently attacked by native herbivores. Growth and leaf damage were significantly higher for invasive populations than for native populations. Growth of invasive populations was not significantly affected by insecticide spray, but insecticide spray benefited that of native populations. In the bioassay trial, beetles preferentially consumed leaf tissue of invasive populations compared to native populations when beetles had a choice between them. Regression of percent leaf damage on biomass showed that invasive populations tolerated herbivory more effectively than native populations. Our results suggest that S. sebiferum from the introduced range had lower resistance but higher tolerance to specialist herbivores. Both defense strategies could have evolved as a response to the escape from natural enemies in the introduced range.