Chemical and Mechanical Defenses Vary among Maternal Lines and Leaf Ages in Verbascum thapsus L. (Scrophulariaceae) and Reduce Palatability to a Generalist Insect

Intra-specific variation in host-plant quality affects herbivore foraging decisions and, in turn, herbivore foraging decisions mediate plant fitness. In particular, variation in defenses against herbivores, both among and within plants, shapes herbivore behavior. If variation in defenses is genetically based, it can respond to natural selection by herbivores. We quantified intra-specific variation in iridoid glycosides, trichome length, and leaf strength in common mullein (Verbascum thapsus L, Scrophulariaceae) among maternal lines within a population and among leaves within plants, and related this variation to feeding preferences of a generalist herbivore, Trichopulsia ni Hübner. We found significant variation in all three defenses among maternal lines, with T. ni preferring plants with lower investment in chemical, but not mechanical, defense. Within plants, old leaves had lower levels of all defenses than young leaves, and were strongly preferred by T. ni. Caterpillars also preferred leaves with trichomes removed to leaves with trichomes intact. Differences among maternal lines indicate that phenotypic variation in defenses likely has a genetic basis. Furthermore, these results reveal that the feeding behaviors of T. ni map onto variation in plant defense in a predictable way. This work highlights the importance of variation in host-plant quality in driving interactions between plants and their herbivores.     

Herbivore-specific elicitation of photosynthesis by mirid bug salivary secretions in the wild tobacco Nicotiana attenuata

Herbivory is thought to be detrimental to plant fitness and commonly results in a metabolic shift in the plant: photosynthetic processes are typically down-regulated, while resource allocation to defenses is increased in herbivore-attacked plants, resulting in fitness costs of induced plant responses. Wild tobacco, Nicotiana attenuata, attacked by Tupiocoris notatus mirid bugs becomes resistant against more damaging herbivores through mirid-induced direct and indirect defenses. However, mirid-induced resistance and tissue loss do not result in a reduction of plant fitness. These findings suggest induced metabolic responses allowing the plant to compensate for the lost tissue and resources allocated to defenses. While feeding by Manduca sexta larvae results in a strong down-regulation of photosynthesis, we demonstrate a specific induction of elevated photosynthetic activity in N. attenuata leaves by elicitors in mirid salivary secretions. The elevated CO(2) assimilation rate is sufficient to compensate for the loss of photosynthetically active tissue and balances the net photosynthesis of infested leaves. We discuss the observed increase in the plant's primary metabolic activity as a mechanism that allows plants to alleviate negative fitness effects of mirid attack and mediates the vaccination effects that result in a net benefit in environments with multiple herbivores.     

Parasitism by Cuscuta pentagona attenuates host plant defenses against insect herbivores

Considerable research has examined plant responses to concurrent attack by herbivores and pathogens, but the effects of attack by parasitic plants, another important class of plant-feeding organisms, on plant defenses against other enemies has not been explored. We investigated how attack by the parasitic plant Cuscuta pentagona impacted tomato (Solanum lycopersicum) defenses against the chewing insect beet armyworm (Spodoptera exigua; BAW). In response to insect feeding, C. pentagona-infested (parasitized) tomato plants produced only one-third of the antiherbivore phytohormone jasmonic acid (JA) produced by unparasitized plants. Similarly, parasitized tomato, in contrast to unparasitized plants, failed to emit herbivore-induced volatiles after 3 d of BAW feeding. Although parasitism impaired antiherbivore defenses, BAW growth was slower on parasitized tomato leaves. Vines of C. pentagona did not translocate JA from BAW-infested plants: amounts of JA in parasite vines grown on caterpillar-fed and control plants were similar. Parasitized plants generally contained more salicylic acid (SA), which can inhibit JA in some systems. Parasitized mutant (NahG) tomato plants deficient in SA produced more JA in response to insect feeding than parasitized wild-type plants, further suggesting cross talk between the SA and JA defense signaling pathways. However, JA induction by BAW was still reduced in parasitized compared to unparasitized NahG, implying that other factors must be involved. We found that parasitized plants were capable of producing induced volatiles when experimentally treated with JA, indicating that resource depletion by the parasite does not fully explain the observed attenuation of volatile response to herbivore feeding. Collectively, these findings show that parasitic plants can have important consequences for host plant defense against herbivores.     

Co(i)-ordinating defenses: NaCOI1 mediates herbivore- induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses

Arabidopsis and tomato plants mutated in the F-box protein COI1 mediating jasmonate (JA) responses are more susceptible to herbivores in laboratory trials, but the exact mechanisms of COI1-mediated resistance are not known. We silenced COI1 by transformation with an inverted repeat construct (ir-coi1) in Nicotiana attenuata, a plant the direct and indirect defenses of which against various herbivores have been well studied. ir-coi1 plants are male sterile and impaired in JA-elicited direct [nicotine, caffeoylputrescine and trypsin proteinase inhibitor (TPI) activity] and indirect (cis-alpha-bergamotene emission) defense responses; responses not elicited by JA treatment (ethylene production and flower TPI activity) were unaffected. Larvae of Manduca sexta, a common herbivore of N. attenuata, gained three times more mass feeding on ir-coi1 than on wild-type (WT) plants in glasshouse experiments. By regularly moving caterpillars to unattacked leaves of the same plant, we demonstrate that larvae on WT plants can grow and consume leaves as fast as those on ir-coi1 plants, a result that underscores the role of COI1 in mediating locally induced resistance in attacked leaves, and the importance of herbivore movement in avoiding the induced defenses of a plant. When transplanted into native habitats in the Great Basin Desert, ir-coi1 plants suffer greatly from damage by the local herbivore community, which includes herbivores not commonly found on N. attenuata WT plants. Choice assays with field-grown plants confirmed the increased attractiveness of ir-coi1 plants for both common and unusual herbivores. We conclude that NaCOI1 is essential for induced resistance in N. attenuata, and that ir-coi1 plants highlight the benefits of herbivore movement for avoiding induced defenses.     

Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

In plant–arthropod associations, the first herbivores to colonise a plant may directly or indirectly affect community assembly on that particular plant. Whether the order of arrival of different arthropod species further modulates community assembly and affects plant fitness remains unclear. Using wild Brassica oleracea plants in the field, we manipulated the order of arrival of early‐season herbivores that belong to different feeding guilds, namely the aphid Brevicoryne brassicae and caterpillars of Plutella xylostella. We investigated the effect of herbivore identity and order of arrival on community assembly on two B. oleracea plant populations during two growth seasons. For this perennial plant, we evaluated whether foliar herbivory also affected herbivore communities on the flowers and if these interactions affected plant seed production. Aphid infestation caused an increase in parasitoid abundance, but caterpillars modulated these effects, depending on the order of herbivore infestation and plant population. In the second growth season, when plants flowered, the order of infestation of leaves with aphids and caterpillars more strongly affected abundance of herbivores feeding on the flowers than those feeding on leaves. Infestation with caterpillars followed by aphids caused an increase in flower‐feeding herbivores compared to the reversed order of infestation in one plant population, whereas the opposite effects were observed for the other plant population. The impact on plant seed set in the first reproductive year was limited. Our work shows that the identity and arrival order of early season herbivores may have long‐term consequences for community composition on individual plants and that these patterns may vary among plant populations. We discuss how these community processes may affect plant fitness and speculate on the implications for evolution of plant defences.     

Costs and benefits of jasmonic acid induced responses in soybean

In response to herbivory, plants have evolved defense strategies to reduce herbivore preference and performance. A strategy whereby defenses are induced only upon herbivory can mitigate costs of defense when herbivores are scarce. Although costs and benefits of induced responses are generally assumed, empirical evidence for many species is lacking. Soybean (Glycine max L. Merr.) has emerged as a model species with which to address questions about induced responses. To our knowledge, this is the first study to examine the fitness costs and benefits of jasmonic acid-induced responses by soybean in the absence and presence of soybean loopers (Chrysodeix includens Walker) (Lepidoptera: Noctuidae). In a greenhouse experiment we demonstrated that soybean induction was costly. Induced plants produced 10.1% fewer seeds that were 9.0% lighter, and had 19.2% lower germination rates than noninduced plants. However, induction provided only modest benefits to soybeans. In a choice experiment, soybean loopers significantly preferred leaves from noninduced plants, consuming 62% more tissue than from induced plants. Soybean loopers that fed on plants that were previously subjected to treatment with jasmonic acid matured at the same rate and to the same size as those that fed on control plants. However, at high conspecific density, soybean looper survivorship was reduced by 44% on previously induced relative to control plants. Reduced soybean looper preference and survivorship did not translate into fitness benefits for soybeans. Our findings support theoretical predictions of costly induced defenses and highlight the importance of considering the environmental context in studies of plant defense.     

Consequences of the overproduction of methyl jasmonate on seed production, tolerance to defoliation and competitive effect and response of Arabidopsis thaliana

* Accumulation of methyl jasmonate (MeJA) after herbivore attack in plants is associated with the induction of defenses that can benefit fitness, but are costly to express; effects often explored using exogenous application of jasmonates. * Here I explored the consequences of the overexpression of MeJA on seed production, tolerance to defoliation and competitive effect and response, using a genotype of Arabidopsis thaliana that overexpresses jasmonic acid carboxyl methyltransferase (JMT) and contains threefold higher levels of MeJA than wild-type plants. * Without competition, JMT plants produced 37-40% less total seed mass than vector controls or wild-type plants, and had reduced seed germination. Defoliation reduced height more strongly in wild-type than in JMT plants, but reduced total seed production equally. In a competition experiment, the presence of a neighbor reduced fitness more strongly in wild-type than in JMT plants, but JMT plants exhibited dampened opportunity costs and benefits of induction with jasmonic acid of itself or its neighbor. This may have related to the higher constitutive expression but reduced inducibility of jasmonate-mediated defenses, including trypsin inhibitors, exhibited by JMT plants. * In natural plant populations, overexpression of MeJA-mediated responses should be beneficial to resistance to herbivores, pathogens and competitors, but is directly costly to fitness and probably constrains plasticity in response to changing environmental conditions.     

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.     

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

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

Exposure of Unwounded Plants to Chemical Cues Associated with Herbivores Leads to Exposure-Dependent Changes in Subsequent Herbivore Attack

Although chemical predator cues often lead to changes in the anti-predator behavior of animal prey, it is not clear whether non-volatile herbivore kairomones (i.e. incidental chemical cues produced by herbivore movement or metabolism but not produced by an attack) trigger the induction of defense in plants prior to attack. I found that unwounded plants (Brassica nigra) that were regularly exposed to kairomones from snails (mucus and feces produced during movement of Helix aspersa) subsequently experienced reduced rates of attack by snails, unlike unwounded plants that received only one initial early exposure to snail kairomones. A follow-up experiment found that mucus alone did not affect snail feeding on previously harvested B. oleracea leaves, suggesting that changes in herbivory on B. nigra were due to changes in plant quality. The finding that chemicals associated with herbivores leads to changes in palatability of unwounded plants suggests that plants eavesdrop on components of non-volatile kairomones of their snail herbivores. Moreover, this work shows that the nature of plant exposure matters, supporting the conclusion that plants that have not been attacked or wounded nonetheless tailor their use of defenses based on incidental chemical information associated with herbivores and the timing with which cues of potential attack are encountered.     

Entrapped carrion increases indirect plant resistance and intra‐guild predation on a sticky tarweed

Many plants employ indirect defenses against herbivores; often plants provide a shelter or nutritional resource to predators, increasing predator abundance, and lessening herbivory to the plant. Often, predators on the same plant represent different life stages and different species. In these situations intraguild predation (IGP) may occur and may decrease the efficacy of that defense. Recently, several sticky plants have been found to increase indirect defense by provisioning predatory insects with entrapped insects (hereafter: carrion). We conducted observational studies and feeding trials with herbivores and predators on two sticky, insect‐entrapping asters, Hemizonia congesta and Madia elegans, to construct food webs for these species and determine the prevalence of IGP in these carrion‐provisioning systems. In both systems, intraguild predation was the most common interaction observed. To determine whether IGP was driven by resource abundance, whether it reduced efficacy of this indirect defense and whether stickiness or predator attraction was induced by damage, we performed field manipulations on H. congesta. Carrion supplementation led to an increase in predator abundance and IGP. IGP was asymmetric within the predator guild: assassin bugs and spiders preyed on small stilt bugs but not vice versa. Despite increased IGP, carrion provisions decreased the abundance of the two most common herbivores (a weevil and a mealybug). Overall seed set was driven by plant size, but number of seeds produced per fruit significantly increased with increasing carrion, likely because of the reduction in the density of a seed‐feeding weevil. Observationally and experimentally, we found that carrion‐mediated indirect defense of tarweeds led to much intraguild predation, though predators effectively reduced herbivore abundance despite the increase in IGP.     

Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant–plant mutualism?

Many plants use induced defenses to reduce the costs of antiherbivore defense. These plants invest energy in growth when herbivores are absent but shunt energy to defense when herbivores are present. In contrast, constitutive defenses are expressed continuously regardless of herbivore presence. Induction has been widely documented in temperate plants but has not been reported from tropical plants. Most tropical plants have higher, more constant herbivore pressure than temperate plants. In this situation, it is hypothesized that constitutive defenses rather than induced defense would be favored. Using natural herbivores of four species of Inga saplings on Barro Colorado Island, Panama, herbivore presence was crossed with ant presence to determine their effects on extrafloral nectar production. Analysis of nectar samples revealed that Inga species do not induce nectar production in response to herbivores. This result is not due to an inability of the plants to respond, as the plants in this study increased nectar production in response to light and ant presence. Contrary to most induction experiments with temperate ecosystem plants, these results demonstrate that tropical plants do not induce one type of defense, and they suggest that the most adaptive defense strategies are different for the two ecosystems.     

Effector proteins that modulate plant--insect interactions

Insect herbivores have highly diverse life cycles and feeding behaviors. They establish close interactions with their plant hosts and suppress plant defenses. Chewing herbivores evoke characteristic defense responses distinguishable from general mechanical damage. In addition, piercing-sucking hemipteran insects display typical feeding behavior that suggests active suppression of plant defense responses. Effectors that modulate plant defenses have been identified in the saliva of these insects. Tools for high-throughput effector identification and functional characterization have been developed. In addition, in some insect species it is possible to silence gene expression by RNAi. Together, this technological progress has enabled the identification of insect herbivore effectors and their targets that will lead to the development of novel strategies for pest resistances in plants.     

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.     

Strong but opposing effects of associational resistance and susceptibility on defense phenotype in an African savanna plant

The susceptibility of plants to herbivores can be strongly influenced by the identity, morphology and palatability of neighboring plants. While the defensive traits of neighbors often determine the mechanism and strength of associational resistance and susceptibility, the effect of neighbors on plant defense phenotype remains poorly understood. We used field surveys and a prickle‐removal experiment in a semi‐arid Kenyan savanna to evaluate the efficacy of physical defenses against large mammalian herbivores in a common understory plant, Solanum campylacanthum. We then quantified the respective effects of spinescent Acacia trees and short‐statured grasses on browsing damage and prickle density in S. campylacanthum. We paired measurements of prickle density beneath and outside tree canopies with long‐term herbivore‐exclusion experiments to evaluate whether associational resistance reduced defense investment by decreasing browsing damage. Likewise, we compared defense phenotype within and outside pre‐existing and experimentally created clearings to determine whether grass neighbors increased defense investment via associational susceptibility. Removing prickles increased the frequency of browsing by ~25%, and surveys of herbivory damage on defended leaves suggested that herbivores tended to avoid prickles. As predicted, associational resistance and susceptibility had opposing effects on plant phenotype: individuals growing beneath Acacia canopies (or, analogously, within large‐herbivore exclosures) had a significantly lower proportion of their leaves browsed and produced ~ 70–80% fewer prickles than those outside refuges, whereas plants in grass‐dominated clearings were more heavily browsed and produced nearly twice as many prickles as plants outside clearings. Our results demonstrate that associational resistance and susceptibility have strong, but opposing, effects on plant defense phenotype, and that variable herbivore damage is a major source of intraspecific variation in defense phenotype in this system.     

Timing of induced resistance in a clonal plant network

After local herbivory, plants can activate defense traits both at the damaged site and in undamaged plant parts such as in connected ramets of clonal plants. Since defense induction has costs, a mismatch in time and space between defense activation and herbivore feeding might result in negative consequences for plant fitness. A short time lag between attack and defense activation is important to ensure efficient protection of the plant. Additionally, the duration of induced defense production once the attack has stopped is also relevant in assessing the cost–benefit balance of inducible defenses, which will depend on the absence or presence of subsequent attacks. In this study we quantified the timing of induced responses in ramet networks of the stoloniferous herb Trifolium repens after local damage by Mamestra brassicae larvae. We studied the activation time of systemic defense induction in undamaged ramets and the decay time of the response after local attack. Undamaged ramets became defense‐induced 38–51 h after the initial attack. Defense induction was measured as a reduction in leaf palatability. Defense induction lasted at least 28 days, and there was strong genotypic variation in the duration of this response. Ramets formed after the initial attack were also defense‐induced, implying that induced defense can extend to new ramet generations, thereby contributing to protection of plant tissue that is both very vulnerable to herbivores and most valuable in terms of future plant growth and fitness.     

Quantifying the response of free-ranging mammalian herbivores to the interplay between plant defense and nutrient concentrations

While trying to achieve their nutritional requirements, foraging herbivores face the costs of plant defenses, such as toxins. Teasing apart the costs and benefits of various chemical constituents in plants is difficult because their chemical defenses and nutrient concentrations often co-vary. We used an approach derived from predator–prey studies to quantitatively compare the foraging response of a free-ranging mammalian herbivore, the swamp wallaby (Wallabia bicolor), through three feeding trials with artificial diets that differed in their concentrations of (1) the terpene 1,8-cineole, (2) primary constituents (including nitrogen and fiber), and (3) both the terpene and the primary constituents. Applying the giving-up density (GUD) framework, we demonstrated that the foraging cost of food patches increases with higher dietary cineole concentration and decreases with higher dietary nutrient concentration. The effect of combined differences in nutrients and cineole concentrations on GUD was interactive, and high nutrient food required more cineole to achieve the same patch value as low nutrient food. Our results indicate that swamp wallabies equate low nutrient, poorly defended food with high nutrient, highly defended food, providing two contrasting diets with similar cost–benefit outcomes. This behavior suggests that equal concentrations of chemical defenses provide nutrient-poor plants with relatively greater protection as nutrient-rich plants. Nutrient-rich plants may therefore face the exacerbated problem of being preferred by herbivores and therefore need to produce more defense compounds to achieve the same level of defense as nutrient-poor plants. Our findings help explain the difference in anti-herbivore strategy of nutrient-poor and rich plants, i.e., tolerance versus defense.     

Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation

1. Fungal endophytes are ubiquitous associates of virtually all plant species. Although many studies have focused on the role of these microorganisms as mediators of plant–herbivore interactions, these studies have usually been conducted using short‐term experiments. 2. Truly effective defences against herbivores may require normal functioning of the plant, as excised leaves may be less resistant as compared with those still attached to the plant. Yet, most studies investigating possible effects of endophytes in conferring host resistance to herbivores have been conducted with plant parts rather than intact plants. 3. Using the root endophytic fungus (Acremonium strictum)—broad bean (Vicia faba)—generalist herbivore (Helicoverpa armigera) model, we conducted experiments to examine whether endophyte effects on herbivory would depend on the experimental setting used in the investigation and whether they would translate into a subsequent generation of the herbivore. 4. Acremonium strictum negative effects on the fitness of H. armigera first generation were more evident when the larvae foraged freely on inoculated intact whole plants than when offered leaf discs of inoculated plants. Furthermore, these effects were carried over into H. armigera second generation reared on an artificial diet. 5. Acremonium strictum could not be re‐isolated from V. faba leaves; hence direct contact between the endophyte and the insect could be excluded. Alternatively, loss of volatiles or inhibitory effects of compounds that were stronger in situ might have caused changes in larval feeding and performance on leaf discs as compared with intact plants, regardless of infection status. 6. We suggest that the reduction in fitness parameters of H. armigera across two generations is caused indirectly via an endophyte‐triggered reduction in plant quality.     

Manduca sexta experience high parasitoid pressures in the field but minor fitness costs of consuming plant secondary compounds

1. Plant‐herbivore coevolutionary interactions have led to a range of plant defenses that minimize insect damage and a suite of counter adaptations that allow herbivores to feed on defended plants. Consuming plant secondary compounds results in herbivore growth and developmental costs but can have beneficial effects such as deterrence or harm of parasitoid enemies. Therefore, the role of secondary compounds on herbivore fitness must be considered in the context of the abundance and level of harm from natural enemies and the costs herbivores incur feeding on plant secondary compounds.
2. In this study, I combined field measurements of Cotesia congregata wasp parasitism pressure with detailed measurements of the costs of plant secondary compounds across developmental stages in the herbivore host, Manduca sexta.
3. I show that C. congregata parasitoids exert large negative selective pressures, killing 31%–57% of M. sexta larvae in the field. Manduca sexta developed fastest during instars most at risk for parasitoid oviposition but growth was slowed by consumption of plant secondary compounds. The negative effects of consuming plant secondary compounds as larvae influenced adult size traits but there were no immune, survival, or fecundity costs.
4. These results suggest that developmental costs experienced by M. sexta herbivores consuming defensive compounds are minor in comparison to the strong negative survival pressures from abundant parasitoid enemies.

     

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.