Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect?

Herbivory has many effects on plants, ranging from shifts in primary processes such as photosynthesis, growth, and phenology to effects on defense against subsequent herbivores and other species interactions. In this study, I investigated the effects of herbivory on seed and seedling characteristics of several families of wild radish (Raphanus raphanistrum) to test the hypothesis that herbivory may affect the quality of offspring and the resistance of offspring to plant parasites. Transgenerational effects of herbivory may represent adaptive maternal effects or factors that constrain or amplify natural selection on progeny. Caterpillar (Pieris rapae) herbivory to greenhouse-grown plants caused plants in some families to produce smaller seeds and those in other families to produce larger seeds compared with undamaged controls. Seed mass was positively associated with probability of emergence in the field. The number of setose trichomes, a putative plant defense, was higher in the progeny of damaged plants in some families and lower in the progeny of damaged plants in other families. In a field experiment, plant families varied in their resistance to several herbivores and pathogens as well as in growth rate and time to flowering. Seeds from damaged parent plants were more likely to become infested with a plant virus. Although herbivory on maternal plants did not directly affect interactions of offspring with other plant parasites, seed mass influenced plant resistance to several attackers. Thus, herbivory affected seed characters, which mediated interactions between plants and their parasites. Finally, irrespective of seed mass, herbivory on maternal plants influenced components of progeny fitness, which was dependent on plant family. Natural selection may act on plant responses to herbivory that affect seedling-parasite interactions and, ultimately, fitness.     

The role of interactions between trophic levels in determining the effects of UV-B on terrestrial ecosystems

Understanding the potential impact of ozone depletion on terrestrial ecosystems is constrained by lack of information on the effects of environmentally realistic UV-B doses on terrestrial organisms other than higher plants. Increasing UV-B may alter interactions between plants and consumers through direct effects on consumer organisms (herbivores, phytopathogens, decomposers, etc.). The effects of increasing UV-B on arthropods are not known. Significant UV-B effects on fungi have been reported, and may be either negative (inhibition of spore germination and mycelial growth) or positive (increased growth, induction of reproductive development and sporulation). However, in many cases consumers are unlikely to be directly exposed to UV-B in the field. In addition, UV action spectra for fungi suggest that this major group may be less sensitive to the effects of ozone depletion than higher plants. Host mediated effects of UV-B on consumers may include alterations in plant chemistry. While secondary metabolites such as phenolics may increase under increased UV-B, this is not invariably the case and evidence that such changes have significant effects on consumers is limited. In particular, there is no evidence that increased UV-B increases resistance of higher plants to fungal pathogens. Indeed, increased UV-B prior to inoculation results in no significant effect or increased disease. Such responses may be attributable to UV-B effects on host surface properties or on compounds other than phenolics. However, such changes are poorly known, and their potential effects on phytopathogens, herbivores or decomposers cannot be assessed. Understanding the effects of UV-B on terrestrial ecosystems is further limited since virtually nothing is known of possible impacts on higher trophic levels, i.e. predators, parasites or pathogens.     

Patterns of virulence and benevolence in insect‐borne pathogens of plants

Direct and indirect interactions between insect‐borne pathogens and their host plants are reviewed in the context of theoretical analyses of the evolution of virulence. Unlike earlier theories, which maintained that parasites should evolve to be harmless or even beneficial to their hosts, recent models predict that coevolution between pathogen and host may lead to virulence or avirulence, depending on the pathogen transmission system. The studies reviewed here support the hypothesis that virulence can be advantageous for insect‐borne pathogens of plants. Virulent pathogens may be transmitted more readily by vector insects and are likely to induce stronger disease symptoms, thereby potentially making the plant more attractive to vectors. In contrast, the transmission advantage of virulence for seed‐transmitted pathogens is lower and the costs of virulence are high. Pathogens may sometimes benefit plants via indirect interactions that arise through relationships with other organisms. Evidence for the effects of insect‐borne pathogens on plant competition, herbivory, and parasitism also is reviewed, but few studies have measured the outcome of both direct and indirect interactions. Benefits of pathogen infection that accrue to plants from indirect interactions may sometimes outweigh the direct detrimental effects of virulence.     

Marine-terrestrial contrasts in the ecology of plant chemical defenses against herbivores

Small marine herbivores that live on the plants they consume often selectively eat seaweeds that are chemically defended from fishes. Their feeding is unaffected or stimulated by the plant metabolites that deter fishes, and these small herbivores dramatically reduce their susceptibility to predation by associating with host plants that are noxious to fishes. Ecological similarities between these small marine herbivores and numerous terrestrial insects suggest that herbivorous insects also may have evolved a preference for toxic plants because this diminishes their losses to predators, parasites and pathogens. Although marine and terrestrial plants and herbivores evolved in strikingly different environments, the ease of experimentation in some marine systems makes them ideal for addressing certain questions of fundamental importance to both terrestrial and marine workers.     

Herbivores and the evolution of the semelparous perennial life-history of plants

The relationship between a plant and its potential enemies changes drastically after reproduction has started. Using a dynamic modelling approach we study the effects of herbivores and pathogens, that are attracted by reproducing plants, on optimal allocation of resources, and life-history strategies. We assume that the level of attack increases with the investment in reproduction, which may lead to a reduction of current years reproductive success, a reduction of storage efficiency or an increase of plant mortality. If herbivores or pathogens attracted by flowering plants mainly reduce current years reproductive success, the optimal life-history is annual or iteroparous perennial if the attack is an all or nothing event. If the level of consumption increases with the number of herbivores attracted, the optimal life-history is most likely iteroparity with or without mast years. Only under very restricted conditions this may lead to semelparity. If herbivores mainly reduce the efficiency of the resources stored for next year, the optimal life-history is iteroparity. If herbivores mainly reduce survival, the optimal solution is likely to be mast years or semelparity. For parameter values that are realistic for Cynoglossum officinale, a semelparous perennial from calcereous soils, the model predicts that reproduction should start in the third year and that 99% of the available resources at the end of season should be invested in reproduction and only 1% saved for growth next year. With such an investment only c. 1% of the plants would survive after reproduction, so the optimal life-history is close to semelparity. For the small fraction of plants that reproduce more than once, years of vegetative growth only and years with reproduction should alternate. Multiple reproduction is rare in C. officinale. However, such a life history is very common for plants known as semelparous perennial. Although the available empirical evidence is, as yet, circumstantial rather than conclus ive we propose that reproduction related mortality mediated through herbivores or pathogens may play a role in the evolution of the semelparous perennial life-history.     

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.     

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.     

Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities

Background Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence.Scope The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities “inhabiting” a plant.Conclusions Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant’s resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.     

Plant volatiles as method of communication

Plants emit volatile compounds that can act as a communication method to insects, neighboring plants and pathogens. Plants respond to leaf and root damage by herbivores and pathogens by emitting these compounds. The volatile compounds can deter the herbivores or pathogens directly or indirectly by attracting their natural enemies to kill them. The simultaneous damage of plants by herbivores and pathogens can influence plant defense. The induced plant volatiles can also make neighboring plants ready for defense or induce defense in parts distant from the damaged area of the same plant. Belowground root herbivory can alter the defense response to aboveground leaf herbivory. In addition, most plants normally emit volatile compounds from their flowers that directly attract foraging mutualistic insects for nectar, which in turn perform the very important function of pollination for subsequent reproduction. The volatile compounds emitted from the floral and vegetative parts of plants belong to three main classes of compounds: terpenoids, phenylpropanoids/benzenoids, and C6-aldehydes (green-leaf volatiles). The volatile phytohormones methyl salicylate and methyl jasmonate serve as important signaling molecules for communication purposes, and interact with each other to optimize the plant defense response. Here we discuss and integrate the current knowledge on all types of communication between plants and insects, neighboring plants and pathogens that are mediated through plant volatiles.     

Vector and virus induce plant responses that benefit a non-vector herbivore

The negative cross-talk between induced plant defences against pathogens and arthropod herbivores is exploited by vectors of plant pathogens: a plant challenged by pathogens reduces investment in defences that would otherwise be elicited by herbivores. This negative cross-talk may also be exploited by non-vector herbivores which elicit similar anti-herbivore defences in the plant. We studied how damage by the thrips Frankliniella occidentalis and/or infection with Tomato spotted wilt virus (TSWV) affect the performance of a non-vector arthropod: the two-spotted spider mite Tetranychus urticae, a parenchym feeder just like F. occidentalis. Juvenile survival of spider mites on plants inoculated with TSWV by thrips was higher than on control and on thrips-damaged plants. However, thrips damage did not reduce spider-mite survival as compared to the control, suggesting that the positive effect of TSWV on spider-mite survival is independent of anti-thrips defence. Developmental and oviposition rates were enhanced on plants inoculated with TSWV by thrips and on plants with thrips damage. Therefore, spider mites benefit from TSWV-infection of pepper plants, but also from the response of plants to thrips damage. We suggest that the positive effects of TSWV on this non-vector species cannot be explained exclusively by cross-talk between anti-herbivore and anti-pathogen plant defences.     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

Tiadinil, a plant activator of systemic acquired resistance, boosts the production of herbivore-induced plant volatiles that attract the predatory mite Neoseiulus womersleyi in the tea plant Camellia sinensis

Plants respond with various defense mechanisms to pathogenic or herbivorous attack. Some chemicals called plant activators that induce the plant defense response against pathogens have been commercially used to protect plants. Here we studied the effects of tiadinil (TDL) on defense mechanisms against herbivores. TDL suppresses pathogenic fungi on tea leaves by inducing defense mechanisms. We used one of the major trophic systems in tea consisting of the herbivorous mite, Tetranychus kanzawai, and the predatory mite, Neoseiulus womersleyi. TDL enhanced the production of herbivore-induced plant volatiles that attract predatory mites. The predatory mites preferred the T. kanzawai-induced volatiles from TDL-treated plants to those produced by untreated plants. These results suggest that TDL activates the plant defense response via an indirect process mediated by plant volatiles that attract natural enemies of the herbivores. In contrast, the oviposition rate, adult maturation rate, and sex ratio of T. kanzawai were not affected by TDL treatment. These results suggest that TDL did not activate any direct defense against the herbivorous mite.     

Above‐ and Belowground Trophic Interactions on Creeping Thistle (Cirsium arvense) in High‐ and Low‐Diversity Plant Communities: Potential for Biotic Resistance?

The capacity of local communities to control introduced plants is called biotic resistance. Biotic resistance has been almost exclusively tested for plant competition and above ground herbivores and pathogens, while neglecting root herbivores and soil pathogens. Here, we present biotic resistance by above- and below ground herbivores in concert, and relate the abundance of the plant enemies to the species diversity of the local plant communities. The study was carried out in a 7-year-old biodiversity field experiment. We used creeping thistle (Cirsium arvense) as a model, and quantified sap-sucking herbivores: above ground aphids, their antagonists, and root-feeding nematodes. As plant diversity treatments, we used field plots sown with high (15 plant species, HSD) or low (4 plant species, LSD) diverse seed mixtures in 1996 and that were not weeded. Creeping thistle became established spontaneously at the start of the experiment. In 2002, in HSD plots, 90 % of the plant community was made up by 11 species, compared to seven species in LSD plots. No differences were found for C. arvense abundance or biomass. Above ground, three aphid species were found on C. arvense-Uroleucon cirsii, Aphis fabae, and Macrosiphum euphorbiae, but the latter was found only in low densities. Significantly more aphid species were found on individual plants in HSD plots. Moreover, in HSD plots, on average 10 % of aphids were parasitized, while no parasitism was observed in LSD plots. In the root zone of C. arvense, significantly more nematodes were found in HSD than in LSD plots, and a significantly higher proportion of those nematodes were plant parasites. The dominant plant parasitic nematode in both treatments was Paratylenchus. We conclude that biotic resistance by natural enemies may be enhanced by plant species diversity, but that above- and below ground sap-sucking herbivores do not necessarily have to respond similarly to the diversity of the surrounding plant community.     

Direct and ecological costs of resistance and tolerance in the stinging nettle

Plant resistance and tolerance to herbivores, parasites, pathogens, and abiotic factors may involve two types of costs. First, resistance and tolerance may be costly in terms of plant fitness. Second, resistance and tolerance to multiple enemies may involve ecological trade-offs. Our study species, the stinging nettle ( Urtica dioica L.) has significant variation among seed families in resistance and tolerance as well as costs of resistance and tolerance to the holoparasitic plant Cuscuta europaea L. Here we report on variation among seed families (i.e. genetic) in tolerance to nutrient limitation and in resistance to both mammalian herbivores (i.e. number of stinging trichomes) and an invertebrate herbivore (i.e. inverse of the performance of a generalist snail, Arianta arbustorum). Our results indicate direct fitness costs of snail resistance in terms of host reproduction whereas we did not detect fitness costs of mammalian resistance or tolerance to nutrient limitation. We further tested for ecological trade-offs among tolerance or resistance to the parasitic plant, herbivore resistance, and tolerance to nutrient limitation in the stinging nettle. Tolerance of nettles to nutrient limitation and resistance to mammalian herbivores tended to correlate negatively. However, there were no significant correlations among resistance and tolerance to the different natural enemies (i.e. parasitic plants, snails, and mammals). The results of this greenhouse study thus suggest that resistance and tolerance of nettles to diverse enemies are free to evolve independently of each other but not completely without direct costs in terms of plant fitness.     

Symbiotic microorganisms, a key for ecological success and protection of plants

Plant-associated microbial diversity encompasses symbionts, protecting their host against various aggressions. Mycorrhizal and rhizospheric microorganisms buffer effects of soil toxic compounds and soil-borne pathogens. Endophytic bacteria and fungi, some of which are vertically inherited through seeds, take part in plant protection by acting directly on aggressive factors (mainly pathogens and herbivores) or by enhancing plant responses. Plant protective microbial symbionts determine the ecological success of plants; they drastically modify plant communities and related trophic webs. This review suggests approaches to improve the inventory of diversity and functions of in situ plant-associated microorganisms.     

Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis

Chemical defense against herbivores is of utmost importance for plants. Primary and secondary metabolites, including non-protein amino acids, have been implicated in plant defense against insect pests. High levels of non-protein amino acids have been identified in certain plant families, including legumes and grasses, where they have been associated with resistance to insect herbivory. Non-protein amino acids can have direct toxic effects via several mechanisms, including misincorporation into proteins, obstruction of primary metabolism, and mimicking and interfering with insect neurological processes. Additionally, certain non-protein amino acids allow nitrogen to be stored in a form that is metabolically inaccessible to herbivores and, in some cases, may act as signals for further plant defense responses. Specialized insect herbivores often possess specific mechanisms to avoid or detoxify non-protein amino acids from their host plants. Although hundreds of non-protein amino acids have been found in nature, biosynthetic pathways and defensive functions have been elucidated in only a few cases. Next-generation sequencing technologies and the development of additional plant and insect model species will facilitate further research on the production of non-protein amino acids, a widespread but relatively uninvestigated plant defense mechanism.     

Gone with the wind: trembling leaves may deter herbivory

Plants employ various defensive tactics against herbivores but are rarely considered to use rapid movements to resist predation. However, the aboveground parts of plants are often forcefully moved by wind and rain. This passive movement has been overlooked as an anti‐herbivore trait. The leaves of many plant species, such as aspens, Indian sacred fig, bamboos, and palms, tremble even in a slight breeze. Leaves that are easily moved by gentle winds can sometimes resist strong winds and may have other benefits as well. In the present study, it is proposed that the movement of such plant leaves physically deters arthropod herbivory and pathogen infection by repelling colonization and oviposition by herbivorous insects. This leads to herbivores and pathogens being dislodged from the plants, and the ensuing death of the herbivores on the ground or at least their recolonization to other plants, as well as the interruption of feeding, intraspecific communication and the mating behaviour of herbivores, thus lowering their performance on the plant or increasing enemy attack of the herbivores. In addition, passive leaf movements may undermine herbivore camouflage and expose them to predation, and may also allow plant volatiles to diffuse efficiently to repel herbivores and attract natural enemies. Thus, the mechanistic properties of these leaves may have anti‐herbivore effects in the wind and rain. This hypothesis can also be applied to aquatic plants that tremble in gentle water currents. In addition, genetic manipulation of the tendency for leaf movement may be beneficial for the management of pest insects and pathogens with reduced pesticides in forestry and agriculture. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 738–747.     

The effect of nutrients on pyrrolizidine alkaloids in Senecio plants and their interactions with herbivores and pathogens

The aim of this review is to combine the knowledge of studies on effects of nutrients on pyrrolizidine alkaloids (PAs) in Senecio with those studies of effects of PAs on herbivores and pathogens in order to predict the effects that nutrients may have on herbivores and pathogens via changes in PAs. We discuss whether these predictions match with the outcome of studies where the effect of nutrients on herbivores and insects were measured. PA concentrations in S. jacobaea, S. vulgaris and S. aquaticus were mostly reduced by NPK fertilization, with genotype-specific effects occurring. Plant organs varied in their response to increased fertilization; PA concentrations in flowers remained constant, while shoot and roots were mostly negatively affected. Biomass change is probably largely responsible for the change in concentrations. Nutrients affect both the variety and the levels of PAs in the plant. The reduced PA concentrations after NPK fertilization was expected to benefit herbivores, but no or negative responses from insect herbivores were observed. Apparently other changes in the plant after fertilization are overriding the effect of PAs. Pathogens do seem to benefit from the lower PA concentrations after fertilization; they were more detrimental to fertilized plants than to unfertilized control plants. Future studies should include the effect of each element of nutrients separately and in combinations in order to gain more insight in the effect of specific nutrients on PA content in Senecio plants.     

Assessing the biosecurity risk from pathogens and herbivores to indigenous plants: lessons from weed biological control

Some potentially invasive herbivores/pathogens in their home range may attack plants originating from another geographic area. Methods are required to assess the risk these herbivores/pathogens pose to these plants in their indigenous ecosystems. The processes and criteria used by weed biological control researchers to assess the impact of potential biological control agents on a plant species in its non-native range provide a possible framework for assessing risks to indigenous plants. While there are similarities between these criteria such as the need for clear objectives, studies in the native range of the herbivore/pathogen, good knowledge of the ecology of the target plant and taxonomy of the plant and herbivore/pathogen, and modelling of the interaction between the two organisms, there are some important differences in approach. These include the need to consider the threat classification of the plant, the likely greater risk from polyphagous herbivores/pathogens than oligophagous or monophagous species, and the need to consider the impact of an additional natural enemy in conjunction with a suite of existing natural enemies. The costs of conducting a risk assessment of a herbivore/pathogen in another country that damages plants indigenous to another geographic area means that criteria will be needed for deciding which foreign herbivore/pathogen species should be assessed. These criteria could include the threat classification of the plant, the amount of damage to the particular plant organs affected, and the importance in key ecosystems.     

Herbivore benefits from vectoring plant virus through reduction of period of vulnerability to predation

Herbivores can profit from vectoring plant pathogens because the induced defence of plants against pathogens sometimes interferes with the induced defence of plants against herbivores. Plants can also defend themselves indirectly by the action of the natural enemies of the herbivores. It is unknown whether the defence against pathogens induced in the plant also interferes with the indirect defence against herbivores mediated via the third trophic level. We previously showed that infection of plants with Tomato spotted wilt virus (TSWV) increased the developmental rate of and juvenile survival of its vector, the thrips Frankliniella occidentalis. Here, we present the results of a study on the effects of TSWV infections of plants on the effectiveness of three species of natural enemies of F. occidentalis: the predatory mites Neoseiulus cucumeris and Iphiseius degenerans, and the predatory bug Orius laevigatus. The growth rate of thrips larvae was positively affected by the presence of virus in the host plant. Because large larvae are invulnerable to predation by the two species of predatory mites, this resulted in a shorter period of vulnerability to predation for thrips that developed on plants with virus than thrips developing on uninfected plants (4.4 vs. 7.9 days, respectively). Because large thrips larvae are not invulnerable to predation by the predatory bug Orius laevigatus, infection of the plant did not affect the predation risk of thrips larvae from this predator. This is the first demonstration of a negative effect of a plant pathogen on the predation risk of its vector.