Parasitoids follow herbivorous insects to a novel host plant,generalist predators less so

The ‘enemy‐free space’ hypothesis predicts that herbivorous insects can escape their natural enemies by switching to a novel host plant, with consequences for the evolution of host plant specialisation. However, if natural enemies follow herbivores to their novel host plants, enemy‐free space may only be temporary. We tested this by studying the colonisation of the introduced tree Eucalyptus grandis (Hill) Maiden (Myrtaceae) by insects in Brazil, where various species of herbivores have added eucalyptus to their host plant range, which consists of native myrtaceous species such as guava. Some herbivores, for example, Thyrinteina leucoceraea Ringe (Lepidoptera: Geometridae), cause outbreaks in eucalyptus plantations but not on guava, possibly because eucalyptus offers enemy‐free space. We sampled herbivores (mainly Lepidoptera species) and natural enemies on eucalyptus and guava and assessed parasitism of Lepidoptera larvae on both host plant species during ca. 2 years. Overall, predators were encountered more frequently on guava than on eucalyptus. In contrast, parasitoids were encountered equally and parasitism rates of Lepidoptera larvae were similar on both host plants. This indicates that herbivores may escape some enemies by moving to a novel host plant. However, this escape may be temporary and may vary with time. We argue that studying temporal and spatial patterns of enemy‐free space and the response of natural enemies to host use changes of their herbivorous prey is essential for understanding the role of natural enemies in the evolution of host plant use by herbivorous arthropods.     

Host plant and the predator Podisus nigrispinus: when the defense compounds of the plant affect the third trophic level

Many herbivorous insects can overcome chemical plant defenses, using the plant's defensive products for their own good, as a defense against predators. Eucalyptus spp. (Myrtaceae), recently introduced in Brazil, are rich in secondary compounds; however, there are reports that these plants have been suffering from population outbreaks of defoliating Lepidoptera in Brazil. The predator Podisus nigrispinus (Dallas) (Hemiptera: Pentatomidae) has been used against herbivorous insects in eucalyptus plantations, but little is known about its establishment in the field. This study aims to investigate whether the effectiveness of this predator may be affected indirectly by compounds of eucalyptus plants, when compared to guava, Psidium guajava L., a Brazilian native species of Myrtaceae. Thus, we evaluated the performance of P. nigrispinus on larvae of Thyrinteina arnobia (Stoll) (Lepidoptera: Geometridae) reared on eucalyptus (exotic species) or guava plants (native species). Podisus nigrispinus performance (reproduction and survival) was better on larvae fed on guava than on larvae fed on eucalyptus. It is possible that the negative effect on the predator's development occurred because of the plants’ secondary compounds appropriated by caterpillars, due to the short coevolutionary history between eucalyptus and the predator. The data suggest that the chemical compounds that could help the plant's defenses against herbivores may also affect their natural enemies, especially when the interaction between plant and natural enemy involves an exotic plant recently introduced into the insect's habitat.     

Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks

In response to feeding by phytophagous arthropods, plants emit volatile chemicals. This is shown to be an active physiological response of the plant and the released chemicals are therefore called herbivore-induced plant volatiles (HIPV). One of the supposed functions of HIPV for the plant is to attract carnivorous natural enemies of herbivores. Depending on which plant and herbivore species interact, blends of HIPV show qualitative and quantitative variation. Hence, one may ask whether this allows the natural enemies to discriminate between volatiles from plants infested by herbivore species that are either suitable or unsuitable as a food source for the natural enemy. Another question is whether natural enemies can also recognise HIPV when two or more herbivore species that differ in suitability as a food source simultaneously attack the same plant species. By reviewing the literature we show that arthropod predators and parasitoids can tell different HIPV blends apart in several cases of single plant–single herbivore systems and even in single plant–multiple herbivore systems. Yet, there are also cases where predators and parasitoids do not discriminate or discriminate only after having learned the association between HIPV and herbivores that are either suitable or non-suitable as a source of food. In this case, suitable herbivores may profit from colonising plants that are already infested by another non-suitable herbivore. The resulting temporal or partial refuge may have important population dynamical consequences, as such refuges have been shown to stabilise otherwise unstable predator–prey models of the Lotka-Volterra or Nicholson-Bailey type.     

Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory

Plants infested with a single herbivore species can attract natural enemies through the emission of herbivore‐induced plant volatiles (HIPVs). However, under natural conditions plants are often attacked by more than one herbivore species. We investigated the olfactory response of a generalist predators Macrolophus caliginosus to pepper infested with two‐spotted spider mites, Tetranychus urticae, or green peach aphid, Myzus persicae, vs. plants infested with both herbivore species in a Y‐tube olfactometer set up. In addition, the constituents of volatile blends from plants exposed to multiple or single herbivory were identified by gas chromatography‐mass spectrometry (GC‐MS). The mirid bugs showed a stronger response to volatiles emitted from plants simultaneously infested with spider mites and aphids than to those emitted from plants infested by just one herbivore, irrespective of the species. Combined with results from previous studies under similar conditions we infer that this was a reaction to herbivore induced plant volatiles. The GC‐MS analysis showed that single herbivory induced the release of 22 additional compounds as compared with the volatiles emitted from clean plants. Quantitative analyses revealed that the amount of volatile blends emitted from pepper infested by both herbivores was significantly higher than that from pepper infested by a single herbivore. Moreover, two unique substances were tentatively identified (with a probability of 94% and 91%, respectively) in volatiles emitted by multiple herbivory damaged plants: α‐zingiberene and dodecyl acetate.     

Fitness consequences of host plant choice: a field experiment

Determining the relative contributions of different ecological factors for herbivore fitness is one key to understanding the ecology and evolution of host plant choice by herbivores. Natural enemies are increasingly being recognized as an important factor: host plants of inferior quality for development may still be used by herbivores if they provide enemy‐free space (EFS). Here we used the tobacco hornworm, Manduca sexta, to experimentally disentangle the effects of natural enemies from the potentially confounding factors of host plant quality, competition and microhabitat. We explored the consequences for both individual components of fitness and total fitness of M. sexta feeding on a typical high quality host plant, tobacco Nicotiana tabacum and a novel, low quality host plant, devil's claw Proboscidea louisianica in an experimental field environment in the presence of a parasitoid natural enemy, Cotesia congregata. Although early larval survival, development and growth rates, final body size and fecundity were all reduced for M. sexta feeding on devil's claw, a high rate of parasitism on tobacco and an absence of parasitism on devil's claw contributed to similar total fitness (net reproductive rate, R₀) across the two host plant species. Our results suggest M. sexta has adopted a novel host plant (devil's claw) outside its typical host range because this host plant provides enemy free space. In addition, oviposition behavior of adult female M. sexta appears to be well suited to exploiting the enemy‐free space on devil's claw; oviposition by M. sexta on devil's claw appears to correspond with seasonal variation in parasitoid abundance.     

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.     

Second and third trophic level effects of differences in plant species reflect dietary specialisation of herbivores and their endoparasitoids

In natural populations, plants demonstrate an array of indirect and direct defence strategies that help to protect them from their herbivores and pathogens. Indirect defences include the release of odours that attract the natural enemies of herbivores, whereas direct defences may include the production of secondary compounds, allelochemicals that impair herbivore development or repel herbivore attack. Although both strategies have been well studied independently, comparatively little attention has been paid to examining the conflict that may arise between indirect and direct defences, such as when the performance of ‘recruited’ parasitoids or predators is negatively affected by plant allelochemicals. Here, we examine the growth and development of polyphagous and oligophagous folivores and their respective endoparasitoids on three crucifer species. One of the species, Brassica oleracea, was recently cultivated, whereas populations of B. nigra and Barbarea vulgaris occur naturally. Additionally, these species possess contrasting life‐history patterns and are also known to exhibit differences in secondary chemistry. The development of the generalist herbivore–parasitoid system was much more variable over the three crucifers than that exhibited by the specialists. Moreover, generalist herbivore and/or parasitoid fitness‐related traits (survival, development time, pupal, or adult size) were much more negatively affected on the wild crucifers than in the specialist association. Our results suggest that the relative importance of direct and indirect defences in plants may rest on the degree of dietary specialisation exhibited by herbivores and their natural enemies, and on the level of toxicity in the plant species under investigation.     

Indirect plant defense against insect herbivores: a review

Plants respond to herbivore attack by launching 2 types of defenses: direct defense and indirect defense. Direct defense includes all plant traits that increase the resistance of host plants to insect herbivores by affecting the physiology and/or behavior of the attackers. Indirect defense includes all traits that by themselves do not have significant direct impact on the attacking herbivores, but can attract natural enemies of the herbivores and thus reduce plant loss. When plants recognize herbivore‐associated elicitors, they produce and release a blend of volatiles that can attract predators, parasites, and other natural enemies. Known herbivore‐associated elicitors include fatty acid–amino acid conjugates, sulfur‐containing fatty acids, fragments of cell walls, peptides, esters, and enzymes. Identified plant volatiles include terpenes, nitrogenous compounds, and indoles. In addition, constitive traits including extrafloral nectars, food bodies, and domatia can be further induced to higher levels and attract natural enemies as well as provide food and shelter to carnivores. A better understanding of indirect plant defense at global and componential levels via advanced high throughput technologies may lead to utilization of indirect defense in suppression of herbivore damage to plants.     

Little evidence for release from herbivores as a driver of plant invasiveness from a multi‐species herbivore‐removal experiment

Enemy release is frequently posed as a main driver of invasiveness of alien species. However, an experimental multi‐species test examining performance and herbivory of invasive alien, non‐invasive alien and native plant species in the presence and absence of natural enemies is lacking. In a common garden experiment in Switzerland, we manipulated exposure of seven alien invasive, eight alien non‐invasive and fourteen native species from six taxonomic groups to natural enemies (invertebrate herbivores), by applying a pesticide treatment under two different nutrient levels. We assessed biomass production, herbivore damage and the major herbivore taxa on plants. Across all species, plants gained significantly greater biomass under pesticide treatment. However, invasive, non‐invasive and native species did not differ in their biomass response to pesticide treatment at either nutrient level. The proportion of leaves damaged on invasive species was significantly lower compared to native species, but not when compared to non‐invasive species. However, the difference was lost when plant size was accounted for. There were no differences between invasive, non‐invasive and native species in herbivore abundance. Our study offers little support for invertebrate herbivore release as a driver of plant invasiveness, but suggests that future enemy release studies should account for differences in plant size among species.     

虫害诱导植物挥发物(HIPVs)对植食性昆虫的行为调控

虫害诱导植物挥发物(herbivore induced plant volatiles,HIPVs)具有植物种类、品种、生育期和部位的特异性,也具有植食性昆虫种类、虫龄、为害程度、为害方式和其他一些环境因子的特异性。由于其释放量明显大于健康植株,因此更易被天敌、害虫以及邻近的植物等所利用,从而调节植物、植食性昆虫与天敌三者之间的相互作用关系,增强植物在自然界的生存竞争能力。本文对HIPVs在植食性昆虫寄主定位行为中的作用、HIPVs对植食性昆虫的种群调控功能及其应用现状2个方面加以综述,并在展望中对目前研究中存在的一些问题进行了探讨。     

The role of resources and natural enemies in determining the distribution of an insect herbivore population

1. Both resources and natural enemies can influence the distribution of a herbivore. The ideal free distribution predicts that herbivores distribute themselves to optimise utilisation of resources. There is also evidence of herbivores seeking out refuges that reduce natural enemy attack (enemy‐free space). Which of these theories predominates in a thistle–tephritid Terellia ruficauda (Diptera: Tephritidae)–parasitoid interaction is examined. 2. The plant, Cirsium palustre, had a contagious distribution approximated by the negative binomial distribution. Terellia ruficauda foraged preferentially and oviposited on isolated plants although its larvae gained neither nutritional benefit nor reduced natural enemy pressure from such behaviour. 3. Parasitoids of T. ruficauda foraged and oviposited more frequently on isolated than on crowded T. ruficauda, resulting in inverse density‐dependent parasitoid attack at all spatial scales examined. Neither the herbivore nor natural enemies distributed themselves according to the predictions of the ideal free distribution and the herbivore did not oviposit to reduce natural enemy attack. 4. Extrapolating from the theoretical predictions of the ideal free distribution and enemy‐free space to the field requires considerable caution. Terellia ruficauda and its parasitoids appear to select their oviposition sites to spread the risk of losses through factors (e.g. mammal herbivory) that may damage dense clusters of C. palustre.     

Olfactory response of four aphidophagous insects to aphid- and caterpillar-induced plant volatiles

Plants damaged by herbivores emit blends of volatile organic compounds (VOCs) that attract the herbivore’s natural enemies. Most work has focussed on systems involving one plant, one herbivore and one natural enemy, though, in nature, plants support multiple herbivores and multiple natural enemies of these herbivores. Our study aimed to understand how different aphid natural enemies respond to aphid-induced VOCs, and whether attraction of the natural enemies that responded to aphid-induced VOCs was altered by simultaneous damage by a chewing herbivore. We used a model system based on Brassica juncea (Brassicaceae), Myzus persicae (Hemiptera: Aphididae) and Plutella xylostella (Lepidoptera: Plutellidae). Ceraeochrysa cubana (Neuroptera: Chrysopidae) did not show preferences for any plant odour, while Cycloneda sanguinea (Coleoptera: Coccinellidae) responded to undamaged plants over air but not to aphid-damaged plants over undamaged plants. Therefore, no further tests were carried out with these two species. Chrysoperla externa (Neuroptera: Chrysopidae) preferred aphid-damaged plants, but not caterpillar-damaged plants, over undamaged plants, and preferred plants damaged by both herbivores over both undamaged plants and aphid-damaged plants. When tested for responses against undamaged plants, Aphidius colemani (Hymenoptera: Braconidae) preferred aphid-damaged plants but not plants damaged by caterpillars. Plants damaged by both herbivores attracted more parasitoids than undamaged plants, but not more than aphid-damaged plants. Thus, multiply damaged plants were equally attractive to A. colemani and more attractive to C. externa than aphid-damaged plants, while C. cubana and C. sanguinea did not respond to aphid-induced VOCs, highlighting how different natural enemies can have different responses to herbivore-damaged plants.     

Compensation behaviour by insect herbivores and natural enemies: its influence on community structure

Insect herbivores feeding on low-quality plants often compensate by increasing their consumption of plant tissue. This usually results in a longer developmental time leading to a higher vulnerability to natural enemies. This has been termed the slow-growth, high-mortality hypothesis. To explore how compensation may shape the species composition of herbivore and natural enemy populations, we present a mathematical model of a tri-trophic system incorporating both the nutritional quality of plants and herbivores, and the compensatory ability of herbivores and their natural enemies. Using this model we predict the abundance of herbivores and natural enemies, and some characteristics of the composition of species of insect communities along a gradient of plant nutritional quality. Specifically, we make the following predictions: 1) In the absence of natural enemies, the abundance of the juvenile herbivores increases with plant quality, and only highly compensating herbivores persist at low plant nutritional quality. 2) If natural enemies are present, the abundance of the juvenile herbivores decreases with increasing plant quality due to more effective suppression by the natural enemies. Poorly compensating herbivores increase while their highly compensating counterparts decrease with lowered plant quality. 3) When the plants have low nutritional quality, natural enemies will only persist when either very highly compensating herbivores are present or if the natural enemy itself is highly compensating. 4) The abundance of adult herbivores in a community with natural enemies can either increase or decrease with increasing plant quality depending on the compensatory abilities of herbivores and natural enemies.     

Prey‐mediated effects of glucosinolates on aphid predators

1. Plant resistance against herbivores can act directly (e.g. by producing toxins) and indirectly (e.g. by attracting natural enemies of herbivores). If plant secondary metabolites that cause direct resistance against herbivores, such as glucosinolates, negatively influence natural enemies, this may result in a conflict between direct and indirect plant resistance. 2. Our objectives were (i) to test herbivore‐mediated effects of glucosinolates on the performance of two generalist predators, the marmalade hoverfly (Episyrphus balteatus) and the common green lacewing (Chrysoperla carnea) and (ii) to test whether intraspecific plant variation affects predator performance. 3. Predators were fed either Brevicoryne brassicae, a glucosinolate‐sequestering specialist aphid that contains aphid‐specific myrosinases, or Myzus persicae, a non‐sequestering generalist aphid that excretes glucosinolates in the honeydew, reared on four different white cabbage cultivars. Predator performance and glucosinolate concentrations and profiles in B. brassicae and host‐plant phloem were measured, a novel approach as previous studies often measured glucosinolate concentrations only in total leaf material. 4. Interestingly, the specialist aphid B. brassicae selectively sequestered glucosinolates from its host plant. The performance of predators fed this aphid species was lower than when fed M. persicae. When fed B. brassicae reared on different cultivars, differences in predator performance matched differences in glucosinolate profiles among the aphids. 5. We show that not only the prey species, but also the plant cultivar can have an effect on the performance of predators. Our results suggest that in the tritrophic system tested, there might be a conflict between direct and indirect plant resistance.     

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp Cotesia glomerata

Extensive research has been conducted to reveal how species diversity affects ecosystem functions and services. Yet, consequences of diversity loss for ecosystems as a whole as well as for single community members are still difficult to predict. Arthropod communities typically are species‐rich, and their species interactions, such as those between herbivores and their predators or parasitoids, may be particularly sensitive to changes in community composition. Parasitoids forage for herbivorous hosts by using herbivore‐induced plant volatiles (indirect cues) and cues produced by their host (direct cues). However, in addition to hosts, non‐suitable herbivores are present in a parasitoid's environment which may complicate the foraging process for the parasitoid. Therefore, ecosystem changes in the diversity of herbivores may affect the foraging efficiency of parasitoids. The effect of herbivore diversity may be mediated by either species numbers per se, by specific species traits, or by both. To investigate how diversity and identity of non‐host herbivores influence the behaviour of parasitoids, we created environments with different levels of non‐host diversity. On individual plants in these environments, we complemented host herbivores with 1–4 non‐host herbivore species. We subsequently studied the behaviour of the gregarious endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) while foraging for its gregarious host Pieris brassicae L. (Lepidoptera: Pieridae). Neither non‐host species diversity nor non‐host identity influenced the preference of the parasitoid for herbivore‐infested plants. However, after landing on the plant, non‐host species identity did affect parasitoid behaviour, whereas non‐host diversity did not. One of the non‐host species, Trichoplusia ni Hübner (Lepidoptera: Noctuidae), reduced the time the parasitoid spent on the plant as well as the number of hosts it parasitized. We conclude that non‐host herbivore species identity has a larger influence on C. glomerata foraging behaviour than non‐host species diversity. Our study shows the importance of species identity over species diversity in a multitrophic interaction of plants, herbivores, and parasitoids.     

Mycorrhiza modulates aboveground tri‐trophic interactions to the fitness benefit of its host plant

1. Arbuscular mycorrhiza (AM), the association of AM fungi and plant roots, may alter morphological and physiological attributes of aboveground plant parts and thereby influence plant‐associated organisms such as herbivores and their natural enemies, predators and parasitoids. 2. The interactions between AM and the players of aboveground tri‐trophic systems have mainly been considered in isolation from each other. The effects of AM on aboveground herbivore–carnivore population dynamics and the consequences to plant fitness are unknown. 3. We explored AM‐induced compensatory mechanisms for AM‐promoted proliferation of the herbivorous spider mite, Tetranychus urticae Koch, on whole bean plants, Phaseolus vulgaris L. Vegetative and reproductive plant growth, AM fungal colonisation levels, and mite densities were assessed on spider mite‐infested plants colonised or not by the AM fungus Glomus mosseae Nicol. & Gerd, and harbouring the natural enemy of the spider mites, the predatory mite Phytoseiulus persimilis Anthias‐Henriot or not. 4. AM symbiosis modulated the aboveground tri‐trophic system to the fitness benefit of the plant. AM‐increased plant productivity outweighed the fitness decrease due to AM‐promoted herbivory: at similar vegetative growth, mycorrhizal plants produced more seeds than non‐mycorrhizal plants. 5. AM‐increased spider mite population levels were compensated for by enhanced population growth of the predators and increased plant tolerance to herbivory. 6. AM‐enhanced predator performance looped back to the AM fungus and stabilised its root colonisation levels, providing the first experimental evidence of a mutually beneficial interaction between AM and an aboveground third trophic level natural enemy.     

Natural enemy impacts on Bemisia tabaci (MEAM1) dominate plant quality effects in the cotton system

1. Plant quality (bottom‐up effects) and natural enemies (top‐down effects) affect herbivore performance. Furthermore, plant quality can also influence the impact of natural enemies. 2. Lower plant quality through reduced irrigation increased the abundance of the cryptic species from the Bemisia tabaci complex [hereafter B. tabaci Middle East Asia Minor 1 (MEAM1)], but not its natural enemies on cotton. It was therefore predicted that lower plant quality would diminish the impact of natural enemies in regulating this herbivore. 3. Over three cotton seasons, plant quality was manipulated via differential irrigation and natural enemy abundance with insecticides. Life tables were used to evaluate the impact of these factors on mortality of immature B. tabaci (MEAM1) over nine generations. 4. Mortality of B. tabaci (MEAM1) was consistently affected by natural enemies but not by plant quality. This pattern was driven by high levels of sucking predation, which was the primary (key) factor associated with changes in immature mortality across all irrigation and natural enemy treatments. Dislodgement (chewing predation and weather) and parasitism contributed as key factors in some cases. Analyses also showed that elimination of sucking predation and dislodgement would have the greatest effect on overall mortality. 5. The top‐down effects of natural enemies had dominant effects on populations of B. tabaci (MEAM1) relative to the bottom‐up effects of plant quality. Effects were primarily due to native generalist arthropod predators and not more host‐specific aphelinid parasitoids. The findings of this study demonstrate the important role of arthropod predators in population suppression and validate the importance of conservation biological control in this system for effective pest control.     

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.     

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

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

Slow‐growth high‐mortality: A meta‐analysis for insects

The slow growth‐high mortality hypothesis (SG‐HG) predicts that slower growing herbivores suffer greater mortality due to a prolonged window of vulnerability. Given diverse plant–herbivore–natural enemy systems resulting from different feeding ecologies of herbivores and natural enemies, this hypothesis might not always be applicable to all systems. This is evidenced by mixed support from empirical data. In this study, a meta‐analysis of the SG‐HM hypothesis for insects was conducted, aiming to find conditions that favor or reject SG‐HM. The analysis revealed significant within‐ and between‐group heterogeneity for almost all explanatory variables and overall did not support SG‐HM. In this analysis, SG‐HM was supported when any of the following 5 conditions was met: (1) host food consisted of artificial diet; (2) herbivore growth was measured as larval mass; (3) herbivores were generalists; (4) no or multiple species of natural enemies were involved in the study; and (5) parasitoids (i.e., parasitic insects) involved in the study were gregarious. SG‐HM was rejected when any of the following 5 conditions was met: (1) herbivores were from the order Hymentoptera; (2) parasitoids from more than 1 order caused herbivore mortality; (2) parasitoids were specialists; (3) parasitoids were solitary; (4) parasitoids were idiobionts or koinobionts; and (5) single species of natural enemy caused mortality of specialist herbivores. All known studies investigated herbivore mortality for a short period of their life cycle. Researchers are encouraged to monitor herbivore mortality during the entire window of susceptibility or life cycle using life tables. Studies involving multiple mortality factors (i.e., both biotic and abiotic) or multiple natural enemy species are also encouraged since herbivores in nature face a multitude of risks during the entire life cycle. More comprehensive studies may increase our understanding of factors influencing the relationships between herbivore growth and mortality.