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

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

Integration of two herbivore‐induced plant volatiles results in synergistic effects on plant defence and resistance

Plants can use induced volatiles to detect herbivore‐ and pathogen‐attacked neighbors and prime their defenses. Several individual volatile priming cues have been identified, but whether plants are able to integrate multiple cues from stress‐related volatile blends remains poorly understood. Here, we investigated how maize plants respond to two herbivore‐induced volatile priming cues with complementary information content, the green leaf volatile (Z)‐3‐hexenyl acetate (HAC) and the aromatic volatile indole. In the absence of herbivory, HAC directly induced defence gene expression, whereas indole had no effect. Upon induction by simulated herbivory, both volatiles increased jasmonate signalling, defence gene expression, and defensive secondary metabolite production and increased plant resistance. Plant resistance to caterpillars was more strongly induced in dual volatile‐exposed plants than plants exposed to single volatiles.. Induced defence levels in dual volatile‐exposed plants were significantly higher than predicted from the added effects of the individual volatiles, with the exception of induced plant volatile production, which showed no increase upon dual‐exposure relative to single exposure. Thus, plants can integrate different volatile cues into strong and specific responses that promote herbivore defence induction and resistance. Integrating multiple volatiles may be beneficial, as volatile blends are more reliable indicators of future stress than single cues.     

Costs of induced volatile production in maize

Herbivore‐induced plant volatiles have been shown to serve as indirect defence signals that attract natural enemies of herbivores. Parasitoids and predators exploit these plant‐provided cues to locate their victims and several herbivores are repelled by the volatiles. Recently, benefits, in terms of plant fitness, from the action of the parasitoids were shown for a few systems. However, the cost of production of herbivore‐induced volatiles for the plant remains unknown. Here, we estimate the fitness cost of the production of induced volatiles in maize, Zea mays. Plants were treated with regurgitant of Spodoptera littoralis or with the elicitor volicitin and we measured dry weight of plant parts at specific times after treatments. After a two‐week treatment period, the dry‐weight of leaves of induced plants was lower than that of un‐induced plants, suggesting a metabolic cost for induced defence. However, maize plants seem to compensate for this loss during subsequent growth, since seed production at maturity was not different for unharmed plants and plants treated with caterpillar regurgitant. For volicitin treated plants a small but significant reduction in seed production was found. It is likely that the treatments also induced the production of other defence compounds, which will contribute to the cost. Yet, a comparison of six maize inbred lines with distinct differences in volatile emissions showed a strong correlation between the intensity of induced emissions and reduction in plant performance. An analysis of the terpenoids that accumulated in the leaves of the inbred lines revealed non‐volatilised compounds are constitutively present in maize and only the volatilised compounds are induced. Interestingly, the lines that released the largest amounts of induced volatiles also contained more of the non‐volatile terpenoids. Based on these results and results from a previous study on the benefits of attracting parasitoids, we conclude that costs of induced volatile production in plants are counterbalanced by the benefits as long as natural enemies of the herbivores are present in the environment.     

Consequences of sequential attack for resistance to herbivores when plants have specific induced responses

Plants in nature are attacked sequentially by herbivores, and theory predicts that herbivore-specific responses allow plants to tailor their defenses. We present a novel field test of this hypothesis, and find that specific responses of Solanum dulcamara lead to season-long consequences for two naturally colonizing herbivores, irrespective of the second herbivore to attack plants. This result indicates that responses induced by the initial herbivore made plants less responsive to subsequent attack. We show that initial herbivory by flea beetles and tortoise beetles induce distinct plant chemical responses. Initial herbivory by flea beetles lowered the occurrence of conspecifics and tortoise beetles relative to controls. Conversely, initial herbivory by tortoise beetles did not influence future herbivory. Remarkably, the experimentally imposed second herbivore to feed on plants did not modify consequences (induced resistance or lack thereof) of the first attacker. Induction of plant chemical responses was consistent with these ecological effects; i.e. the second herbivore did not modify the plant's initial induced response. Thus, canalization of the plant resistance phenotype may constrain defensive responses in a rapidly changing environment.     

Beta and habitat diversity in marine systems: a new approach to measurement, scaling and interpretation

Specialist herbivores are known to alter their host's wound-induced responses but the beneficiaries of these alterations are unknown. Nicotiana attenuata plants release a burst of ethylene specifically in response to feeding by Manduca sexta larvae, which is known to suppress wound- and methyl jasmonate (MeJA)-inducible nicotine accumulation. The ethylene burst may be a mechanism by which M. sexta larvae feed "stealthily" on their host plants or, alternatively, it may allow the plant to optimize its defense response against this specialist herbivore by reducing costs of induction. We examined the impact of the ethylene burst on defense-related fitness costs that are readily observed when plants are treated with MeJA and grown in competition with untreated plants. We elicited nicotine induction (with MeJA), the ethylene burst (with the ethylene releasing compound, ethephon) and inhibited the plant's ability to perceive ethylene (with applications of an antagonist of ethylene receptors, 1-methylcyclopropene, 1-MCP). By simultaneously applying MeJA and ethephon we mimicked the plant's hormonal response to larval attack. We hypothesized that if the ethylene burst benefited the plant, the fitness costs of MeJA induction should be reduced by ethephon and restored if the plants were additionally treated with 1-MCP. In a second experiment, we applied larval oral secretion (OS) to elicit endogenous hormone production and predicted that the 1-MCP treatment should reduce the fitness of OS-treated plants. Our measures of plant fitness, namely the rate of stalk elongation and lifetime capsule production, supported these predictions. We conclude that the ethylene burst elicited by this specialist herbivore can reduce MeJA-induced fitness costs and increase the competitive strength of OS-treated plants. Suppressed nicotine production is likely to contribute to, but is not sufficient to explain, the observed fitness outcomes. The intensity of intra-specific competition and herbivore attack will likely determine the adaptive value of the M. sexta-elicited ethylene response.     

Plants on red alert: do insects pay attention?

Two recent hypotheses have proposed that non-green plant colouration evolved as a defence against herbivores, either as protective colouration promoting handicap signals indicating plant fitness or by undermining their crypsis. The handicap hypothesis posits a co-evolutionary process between plants and herbivores, whereas the anti-crypsis hypothesis suggests that an arms race between insects and plants is the evolutionary mechanism. Both explanations assume that insects are the evolutionary origin causing plants' colouration. Here, we propose a different hypothesis, termed the "Defence Indication hypothesis". This idea focuses on the multiple protective functions of anthocyanins and carotenoids as pigments, and suggests that plant colouration evolved primarily in response to various stressors. Because pigments and defensive compounds share a common biosynthesis, the production of pigments also provides elevated defensive strengths against herbivores, a process termed priming. In effect, the Defence Indication hypothesis predicts that pleiotropic effects of the pigments and, more generally, plants' shared defence responses, explain why insects might react to plant colouration.     

Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study

1.  There are myriad ways in which pollinators and herbivores can interact via the evolutionary and behavioural responses of their host plants.
2.  Given that both herbivores and pollinators consume and are dependent upon plant-derived nutrients and secondary metabolites, and utilize plant signals, plant chemistry should be one of the major factors mediating these interactions.
3.  Here we build upon a conceptual framework for understanding plant-mediated interactions of pollinators and herbivores. We focus on plant chemistry, in particular plant volatiles and aim to unify hypotheses for plant defence and pollination. We make predictions for the evolutionary outcomes of these interactions by hypothesizing that conflicting selection pressures from herbivores and pollinators arise from the constraints imposed by plant chemistry.
4.  We further hypothesize that plants could avoid conflicts between pollinator attraction and herbivore defence through tissue-specific regulation of pollinator reward chemistry, as well as herbivore-induced changes in flower chemistry and morphology.
5.  Finally, we test aspects of our predictions in a case study using a wild tomato species, Solanum peruvianum , to illustrate the diversity of tissue-specific and herbivore-induced differences in plant chemistry that could influence herbivore and pollinator behaviour, and plant fitness.     

Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective

Most herbivorous arthropods are specialists that feed on one or a few related plant species. To understand why this is so, both mechanistic and functional studies have been carried out, predominantly restricted to bitrophic aspects. Host-selection behaviour of herbivorous arthropods has been intensively studied and this has provided ample evidence for the role of secondary plant chemicals as source of information in behavioural decisions of herbivores. Many evolutionary studies have regarded co-evolution between plants and herbivores to explain the diversity of secondary plant chemicals and host specialisation of herbivores. However, many cases remain unexplained where herbivores select host plants that are suboptimal in terms of fitness returns. A stimulating paper by Bernays and Graham [(1988) Ecology 69, 886-892)] has initiated a discussion on the need of a multitrophic perspective to understand the evolution of host-plant specialisation by herbivorous arthropods. However, this has hardly resulted in ecological studies on host-selection behaviour that take a multitrophic perspective. Yet, evidence is accumulating that constitutive and induced infochemicals from natural enemies and competitors can affect herbivore behaviour. These cues may constitute important information on fitness prospects, just as plant cues can do. In this paper I selectively review how information from organisms at different trophic levels varies in space and time and how herbivores can integratively exploit this information during host selection. In doing so, research areas are identified that are likely to provide important new insights to explain several of the questions in herbivore host selection that remain unanswered so far. These research areas are at the interface of evolutionary ecology, behavioural ecology and chemical ecology.     

COSTS OF INDUCED RESPONSES AND TOLERANCE TO HERBIVORY IN MALE AND FEMALE FITNESS COMPONENTS OF WILD RADISH

Theory predicts that plant defensive traits are costly due to trade-offs between allocation to defense and growth and reproduction. Most previous studies of costs of plant defense focused on female fitness costs of constitutively expressed defenses. Consideration of alternative plant strategies, such as induced defenses and tolerance to herbivory, and multiple types of costs, including allocation to male reproductive function, may increase our ability to detect costs of plant defense against herbivores. In this study we measured male and female reproductive costs associated with induced responses and tolerance to herbivory in annual wild radish plants (Raphanus raphanistrum). We induced resistance in the plants by subjecting them to herbivory by Pieris rapae caterpillars. We also induced resistance in plants without leaf tissue removal using a natural chemical elicitor, jasmonic acid; in addition, we removed leaf tissue without inducing plant responses using manual clipping. Induced responses included increased concentrations of indole glucosinolates, which are putative defense compounds. Induced responses, in the absence of leaf tissue removal, reduced plant fitness when five fitness components were considered together; costs of induction were individually detected for time to first flower and number of pollen grains produced per flower. In this system, induced responses appear to impose a cost, although this cost may not have been detected had we only quantified the traditionally measured fitness components, growth and seed production. In the absence of induced responses, 50% leaf tissue removal, reduced plant fitness in three out of the five fitness components measured. Induced responses to herbivory and leaf tissue removal had additive effects on plant fitness. Although plant sibships varied greatly (49–136%) in their level of tolerance to herbivory, costs of tolerance were not detected, as we did not find a negative association between the ability to compensate for damage and plant fitness in the absence of damage. We suggest that consideration of alternative plant defense strategies and multiple costs will result in a broader understanding of the evolutionary ecology of plant defense.     

COST OF GLANDULAR TRICHOMES,A “RESISTANCE” CHARACTER IN DATURA WRIGHTII REGEL (SOLANACEAE)

Models regarding the evolution of plant resistance to herbivory often assume that the primary mechanism maintaining resistance polymorphisms is the balance between benefits of increased resistance to herbivores and costs associated with the production of a resistance character. However, rarely has it been demonstrated that genetically based resistance traits are costly. Here, we document costs associated with the production of glandular trichomes, a resistance character in Datura wrightii that is predominantly under the control of a single gene of large effect. In the absence of herbivores, plants with glandular trichomes (sticky) produced 45% fewer viable seeds than plants with nonglandular trichomes (velvety). Although both plant types flowered with similar frequency, sticky plants matured fewer capsules and fewer of their seeds germinated. The fitness difference between the types in herbivore-free conditions was not mitigated by the addition of water, a potentially limiting resource for sticky plants. Under herbivore pressure, there was no significant fitness difference between the types, although the fitness of velvety plants was still higher than that of sticky plants. This occurred even though velvety plants sustained more herbivore damage than sticky plants and were more likely to be attacked by most herbivore species present. The fitness difference between the plant types was especially reduced when herbivore-attacked plants were watered, which indicates that sticky plants may have higher tolerance for damage than velvety plants when supplied with a potentially limiting resource. Yet, the maintenance of a fitness deficit (albeit small and nonsignificant) for sticky plants when attacked by herbivores indicates no net benefit associated with the production of glandular trichomes in this first year of our study. These results add to our current understanding that herbivore resistance characters can be costly and raise the question of how this genetic polymorphism is maintained in wild populations.     

Herbivore‐induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.     

Herbivore-induced plant volatiles mediate behavioral interactions between a leaf-chewing and a phloem-feeding herbivore

Plants respond adaptively to herbivore stress in order to maintain fitness. Upon herbivore attack, plants emit blends of volatile organic compounds (VOCs) that differ from those that are constitutively emitted. These defense responses are typically specific to the identity of the attacking herbivore and often linked to the herbivore's feeding guild (e.g. chewing, phloem-feeding). Herbivores use plant volatiles to locate suitable host plants and changes in volatile emissions can affect host-plant location. Therefore, herbivores from separate feeding guilds can interact indirectly through the modulation of plant responses. In this study we tested how damage by an herbivore from one feeding guild affected the host-plant choice of an herbivore from a separate feeding guild, and vice versa. A chewing herbivore, the Colorado potato beetle (Leptinotarsa decemlineata), and a phloem feeding herbivore, the green peach aphid (Myzus persicae), were assayed in olfactometers to assess behavioral responses to odors emitted by potato plants (Solanum tuberosum) that were damaged by herbivores from the other feeding guild. Leptinotarsa decemlineata oriented more frequently towards undamaged plants compared to M. persicae damaged plants. Surprisingly, M. persicae preferred plants that were damaged by L. decemlineata, although previous studies had shown that they perform worse on these plants. Distinct differences were detected in the volatile profiles of herbivore-damaged and undamaged plants. Leptinotarsa decemlineata induced stronger volatile emissions compared to undamaged control plants, while M. persicae tended to suppress volatile emissions. These herbivores demonstrate contrasting induction of plant volatiles and behavioral responses. Exploring the nature of co-occurring herbivores and how they perceive potential hosts can play a significant role in understanding the ecological functions and community dynamics of plant plasticity and interactions with a variety of herbivores.     

Between-Population Outbreeding Affects Plant Defence

Between-population crosses may replenish genetic variation of populations, but may also result in outbreeding depression. Apart from direct effects on plant fitness, these outbreeding effects can also alter plant-herbivore interactions by influencing plant tolerance and resistance to herbivory. We investigated effects of experimental within- and between-population outbreeding on herbivore resistance, tolerance and plant fitness using plants from 13 to 19 Lychnis flos-cuculi populations. We found no evidence for outbreeding depression in resistance reflected by the amount of leaf area consumed. However, herbivore performance was greater when fed on plants from between-population compared to within-population crosses. This can reflect outbreeding depression in resistance and/or outbreeding effects on plant quality for the herbivores. The effects of type of cross on the relationship between herbivore damage and plant fitness varied among populations. This demonstrates how between-population outbreeding effects on tolerance range from outbreeding depression to outbreeding benefits among plant populations. Finally, herbivore damage strengthened the observed outbreeding effects on plant fitness in several populations. These results raise novel considerations on the impact of outbreeding on the joint evolution of resistance and tolerance, and on the evolution of multiple defence strategies.     

Latitudinal variation in resistance and tolerance to herbivory of a salt marsh shrub

Interactions between plants and herbivores often vary on a geographic scale. Although theory about plant defenses and tolerance is predicated on temporal or spatial variation in herbivore damage, no single study has compared the pattern of herbivory, plant defenses and tolerance to herbivory of a single species across a latitudinal gradient. In 2002–2005 we surveyed replicate salt marshes along the Atlantic coast of the United States from Florida to Maine. At each field site we scored leaves of Iva frutescens for herbivore damage. In laboratory experiments we measured constitutive resistance and induced resistance in I. frutescens from high and low latitude sites along the Atlantic Coast. In another common garden experiment we studied tolerance to herbivory of I. frutescens from various sites. Theory predicts that constitutive resistance should matter more when damage is high, and induced resistance when herbivory is high but variable. In the field, average levels of herbivore damage, and spatial and temporal variation in herbivore damage were all greater at low versus high latitudes, indicating that constitutive as well as induced resistance should be stronger at low latitudes. Consistent with this prediction, constitutive resistance to herbivory was stronger at low latitudes. Induced resistance to herbivores was also stronger at low latitudes: it was deployed faster and lasted longer. Theory also predicts that tolerance to herbivory should be greater where average herbivory damage is greater; however, tolerance to herbivory in Iva did not depend on geographic origin. Our results emphasize the value of considering multiple ways in which plants respond to herbivores when examining geographic variation in plant–herbivore interactions.     

Jasmonate-mediated induced plant resistance affects a community of herbivores

1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well‐documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well‐developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field. 2. Several proteins that are induced in tomato foliage following herbivore damage have been linked causally to reductions in herbivore performance under laboratory conditions. Application of jasmonic acid, a natural elicitor of these defensive proteins, to tomato foliage stimulates induced responses to herbivory. 3. Jasmonic acid was sprayed on plants in three doses to generate plants with varying levels of induced responses, which were measured as increases in the activities of proteinase inhibitors and polyphenol oxidase. 4. Field experiments conducted over 3 years indicated that induction of these defensive proteins is associated with decreases in the abundance of all four naturally abundant herbivores, including insects in three feeding guilds, caterpillars, flea beetles, aphids, and thrips. Induced resistance killed early instars of noctuid caterpillars. Adult flea beetles strongly preferred control plants over induced plants, and this effect on host plant preference probably contributed to differences in the natural abundance of flea beetles. 5. The general nature of the effects observed in this study suggests that induced resistance will suppress many members of the herbivore community. By linking plant biochemistry, insect preference, performance, and abundance, tools can be developed to manipulate plant resistance sensibly and to predict its outcome under field conditions.     

Temporal consistency in herbivore responses to glucosinolate polymorphism in populations of wild cabbage (Brassica oleracea)

Natural populations of wild cabbage (Brassica oleracea) show significant qualitative diversity in heritable aliphatic glucosinolates, a class of secondary metabolites involved in defence against herbivore attack. One candidate mechanism for the maintenance of this diversity is that differential responses among herbivore species result in a net fitness balance across plant chemotypes. Such top-down differential selection would be promoted by consistent responses of herbivores to glucosinolates, temporal variation in herbivore abundance, and fitness impacts of herbivore attack on plants varying in glucosinolate profile. A 1-year survey across 12 wild cabbage populations demonstrated differential responses of herbivores to glucosinolates. We extended this survey to investigate the temporal consistency of these responses, and the extent of variation in abundance of key herbivores. Within plant populations, the aphid Brevicoryne brassicae consistently preferred plants producing the glucosinolate progoitrin. Among populations, increasing frequencies of sinigrin production correlated positively with herbivory by whitefly Aleyrodes proletella and negatively with herbivory by snails. Two Pieris butterfly species showed no consistent response to glucosinolates among years. Rates of herbivory varied significantly among years within populations, but the frequency of herbivory at the population scale varied only for B. brassicae. B. brassicae emerges as a strong candidate herbivore to impose differential selection on glucosinolates, as it satisfies the key assumptions of consistent preferences and heterogeneity in abundance. We show that variation in plant secondary metabolites structures the local herbivore community and that, for some key species, this structuring is consistent over time. We discuss the implications of these patterns for the maintenance of diversity in plant defence chemistry.     

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.     

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.     

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.     

Plant chemistry underlies herbivore‐mediated inbreeding depression in nature

The cost of inbreeding (inbreeding depression, ID) is an important variable in the maintenance of reproductive variation. Ecological interactions such as herbivory could modulate this cost, provided that defence traits harbour deleterious mutations and herbivores are responsible for differences in fitness. In the field, we manipulated the presence of herbivores on experimentally inbred and outcrossed plants of Solanum carolinense (horsenettle) for three years. Damage was greater on inbred plants, and ID for growth and fitness was significantly greater under herbivory. Inbreeding reduced phenolic expression both qualitatively (phytochemical diversity) and quantitatively, indicating deleterious load at loci related to the biosynthesis of defence compounds. Our results indicate that inbreeding effects on plant–herbivore interactions are mediated by changes to functional plant metabolites, suggesting that variation in inbreeding could be a predictor of defence trait variation. The magnitude of herbivore‐mediated, ecological ID indicates that herbivores could maintain outcrossing mating systems in nature.