GENETICS OF PHYSIOLOGICAL AND BEHAVIORAL RESISTANCE TO HOST FURANOCOUMARINS IN THE PARSNIP WEBWORM

Depressaria pastinacella, the parsnip webworm, feeds almost exclusively on the flowers and fruits of Pastinaca sativa, the wild parsnip. Resistance to webworms in wild parsnip populations is largely attributable to genetically based variation in furanocoumarin chemistry; by differentially reducing fruit set among chemical phenotypes, parsnip webworms may act as selective agents on wild parsnip populations. To determine whether wild parsnip chemistry can act as a selective agent on webworm populations, it is necessary to establish that resistance mechanisms in the webworm to furanocoumarins are genetically based. In this study, we estimated the amount of genetic variation in behavioral and physiological responses of webworms to parsnip furanocoumarins. Virtually no variation was found among webworm families for feeding preferences for diets varying as much as fourfold in furanocoumarin content. Nor was significant variation found for mean furanocoumarin intake over the assay period, except in one case, in which maternal effects may account for differences among families. In contrast, substantial familial variation existed for cytochrome P450–mediated metabolism of bergapten and xanthotoxin, two host furanocoumarins. The presence of additive genetic variation in metabolism, and the absence of such variation in discriminative feeding behavior, suggests that adaptation to changes in furanocoumarin chemistry, resulting either from changes in the distribution of chemical phenotypes in parsnip populations or from shifts to new chemically different host plants, is likely to be facilitated by physiological rather than behavioral means.     

Chemical barriers to adaptation by a specialist herbivore

Summary Depressaria pastinacella, the parsnip webworm (Lepidoptera: Oecophoridae), feeds throughout eastern North America on Pastinaca sativa (wild parsnip) and few other species. The assumption that specialist herbivores such as the parsnip webworm are adapted to hostplant chemistry, and are therefore unaffected by chemical variation in hostplants, was tested. Flower buds from plants grown first in the greenhouse and then in the field were fed to ultimate instar webworms. Plant phenotype had a significant effect on virtually all webworm food utilization parameters. While nutritional factors (i.e., nitrogen content) were correlated with approximate digestibility, two constituents of the flowers — bergapten and xanthotoxin, both linear furanocoumarins — independently accounted for a significant amount of variation in food utilization indicies. The physiological effects of these furanocoumarins were confirmed in artificial diet experiments. Despite the fact that the two most important furanocoumarins in parsnip flowers relative to webworm feeding and growth are isomers, differing only in the positioning of a methoxy substituent, they have different physiological effects; while xanthotoxin in general has no effect on growth, bergapten decreases growth and digestibility of the diet. These results underscore the need in studies of plant-animal interactions to examine individual chemical components rather than classes of compounds.     

Patterns of furanocoumarin production and insect herbivory in a population of wild parsnip (Pastinaca sativa L.)

Summary Seasonal changes in the distribution and abundance of furanocoumarins in wild parsnip, Pastinaca sativa (Umbelliferae), were examined in a population of plants in Tompkins County, New York. Xanthotoxin, imperatorin and bergapten (linear furanocoumarins) occur in all above-ground parts of the plant; in addition, angelicin and sphondin (angular furanocoumarins) occur in umbels of some individuals. Total furanocoumarin content, as measured by percent dry weight, is greatest in reproductive parts, particularly buds and seeds; variation in concentrations between plants is greatest in vegetative structures (e.g., leaves).Within the plant, the distribution of furanocoumarins is significantly correlated with nitrogen, as opposed to biomass, allocation. In that nitrogen is often a factor limiting the plant growth, furanocoumarins appear to be allocated in proportion to plant tissue value; reproductive structures, obvious contributors to plant fitness, contain over ten times the amount of nitrogen and furanocoumarin contained in vegetative structures such as senescent leaves.Stepwise multiple regression analysis revealed that generalized insect herbivores tend to feed on plants or plant parts low in furanocoumarin content and, correspondingly, low in nitrogen content. Parsnip specialists, notably Depressaria pastinacella (Lepidoptera: Oecophoridae), feed exclusively on umbels, plant parts rich in nitrogen and furanocoumarins; furanocoumarin number and content in fact account for over 60% of the variance in number of umbel feeders. These patterns conform with previous determinations of the toxicological properties of furanocoumarins. Nitrogen is known to affect growth rate, fecundity, longevity and survivorship of insect herbivores; by tolerating or detoxifying furanocoumarins, D. pastinacella can consume plant tissues containing significantly greater amounts of nitrogen than tissues consumed by generalist feeders. That the presence of D. pastinacella on individual plants is correlated with the number of furanocoumarins present is consistent with the hypothesis that parsnip specialists use angular furanocoumarins as host recognition cues.     

Phenotype matching in wild parsnip and parsnip webworms: causes and consequences

According to the geographic mosaic theory of coevolution, selection intensity in interactions varies across a landscape, forming a selection mosaic; interaction traits match at coevolutionary hotspots where selection is reciprocal and mismatch at coldspots where reciprocity is not a factor. Chemical traits play an important role in the interaction between wild parsnip (Pastinaca sativa) and the parsnip webworm (Depressaria pastinacella). Furanocoumarins, produced as plant defenses, are detoxified by the webworms by cytochrome P450 monooxygenases; significant additive genetic variation exists for both furanocoumarin production in the plant and detoxification in the insect, making these traits available for selection. To test the hypothesis that differences in selection intensity affect the distribution of coevolutionary hotspots and coldspots in this interaction, we examined 20 populations of webworms and wild parsnips in Illinois and Wisconsin that varied in size, extent of infestation, proximity to woods (and potential vertebrate predators), and proximity to a chemically distinct alternate host plant, Heracleum lanatum (cow parsnip). Twelve of 20 populations displayed phenotype matching between plant defense and insect detoxification profiles. Of the eight mismatched populations, a logistic regression model related matching probability to two predictors: the presence of the alternate host and average content of xanthotoxin (one of the five furanocoumarins produced by P. sativa). The odds of mismatching were significantly increased by the presence of the alternate host (odds ratio = 15.4) and by increased xanthotoxin content (odds ratio = 6.053). Parsnips growing near cow parsnip displayed chemical phenotypes that were chemically intermediate between cow parsnip and parsnips growing in isolation. Rapid phenotype matching in this system is likely due in part to differential mortality every season; larvae transferred to a plant 30 m or more from the plant on which they developed tended to experience increased mortality over larvae transferred to another umbel on the same plant on which they had developed, and plant populations that mismatched in 2001 displayed a change in chemical phenotype distribution from the previous year. Trait mixing through gene flow is also a likely factor in determining mismatch frequency. Populations from which webworms were eradicated the previous year were all recolonized; in three of seven of these populations, infestation rates exceeded 90%. Our findings, consistent with the geographic mosaic theory, suggest that the presence of a chemically distinct alternate host plant can affect selection intensity in such a way as to reduce the likelihood of reciprocity in the coevolutionary interaction between wild parsnip and the parsnip webworm.     

Generalist and specialist host–parasitoid associations respond differently to wild parsnip (Pastinaca sativa) defensive chemistry

1. Plant defensive chemistry is predicted to have a more negative effect on generalist herbivores and their parasitoids than on specialist herbivores and their parasitoids. 2. This prediction was examined by comparing the effects of the wild parsnip (Pastinaca sativa L.) toxin, xanthotoxin, on a generalist herbivore–parasitoid association [the cabbage looper, Trichoplusia ni Hübner, and its polyembryonic parasitoid, Copidosoma floridanum (Ashmead)] and a specialist herbivore–parasitoid association [the parsnip webworm, Depressaria pastinacella (Duponchel), and its polyembryonic parasitoid, Copidosoma sosares (Walker)]. 3. Copidosoma floridanum brood sizes were smaller and experienced lower survivorship when reared in a host feeding on an artificial diet containing a low concentration of xanthotoxin. No T. ni hosts, parasitised or unparasitised, survived on a diet high in xanthotoxin. In contrast, C. sosares brood size and survivorship were unaffected by the presence of low levels of xanthotoxin in the host diet. Copidosoma sosares experienced reduced brood size and survivorship only when its host consumed a diet containing 15 times the level of xanthotoxin as the diet adversely affecting its congener. 4. The differences in response to xanthotoxin exhibited by C. floridanum and C. sosares are explained partly by a differential reduction in host quality and partly by differential exposure to xanthotoxin in host haemolymph. Unlike D. pastinacella, T. ni experienced reduced pupal weight and survivorship and prolonged developmental time on a low‐xanthotoxin diet. More xanthotoxin passed unmetabolised into the haemolymph of T. ni than into the haemolymph of D. pastinacella.     

CONSTRAINTS ON CHEMICAL COEVOLUTION: WILD PARSNIPS AND THE PARSNIP WEBWORM

The parsnip webworm (Depressaria pastinacella) and the wild parsnip (Pastinaca sativa) together represent a potentially “coevolved” system in that throughout their ranges the plant has relatively few other herbivores and the insect has virtually no other hosts. Individual wild parsnip plants within a central Illinois population vary in their content and composition of furanocoumarins, secondary compounds with insecticidal properties. Half-sib and parent-offspring regression estimates of the heritability of furanocoumarins demonstrate that this variation is genetically based. Wild parsnip plants also vary in their resistance to damage by the parsnip webworm, which feeds on flowers and developing seeds. In an experimental garden, seed production in the primary umbel ranged from 0 to 1,664 seeds among individuals, and mean seed production of half-sib families ranged from 3.7 seeds to 446.0 seeds. Approximately 75% of the variation in resistance among half-sib families to D. pastinacella was attributable to four furanocoumarin characteristics—resistance is positively related to the proportion of bergapten and the amount of sphondin in seeds, and negatively related to the amount of bergapten and the proportion of sphondin in leaves. Each of the four resistance factors had significant heritability. Thus, resistance in wild parsnip to the parsnip webworm is to a large extent chemically based and genetically controlled. Genetic correlations among fitness and resistance characters, however, tend to limit coevolutionary responses between herbivore and plant. In greenhouse plants protected from herbivory, several of the resistance factors have negative genetic correlations with potential seed production. Ostensibly, highly resistant plants in the absence of herbivory would be at a competitive disadvantage in the field. The selective impact of the herbivore is also limited in this population by a negative genetic correlation among resistance factors. Selection to increase one resistance factor (e.g., the proportion of bergapten in the seed) would at the same time decrease the amount of a second resistance factor (e.g., the amount of sphondin in the seed). The wild parsnip and the parsnip webworm, then, appear to have reached an evolutionary “stalemate” in the coevolutionary arms race.     

Reduced Aggressive Behavior: A Benefit of Silk-Spinning in the Parsnip Webworm, Depressaria pastinacella (Lepidoptera: Oecophoridae)

The parsnip webworm, Depressaria pastinacella, spins a silken web within the umbels of its host plant, the wild parsnip Pastinaca sativa, and aggressively defends this web against conspecifics. We first established experimentally that the number of aggressive interactions between caterpillars with their webs removed was significantly higher than for webworms with intact webs. In order to determine whether web-spinning acts to divide food resources and reduce aggressive interactions, we measured relative weight gain and total silk production of parsnip webworms isolated from one another, grouped together with webbing undisturbed, and grouped together with webbing removed daily. Parsnip webworms isolated from one another and therefore unable to engage in aggressive interactions attained the highest pupal weights and spun the smallest amount of silk; caterpillars with webs removed daily and therefore with frequent aggressive interactions until territories were reestablished had the lowest pupal weights and spun the greatest quantity of silk. Our findings indicate that, for the parsnip webworm, constructing a silken web reduces aggressive encounters among conspecifics.     

Evolution of tolerance in an invasive weed after reassociation with its specialist herbivore

The interaction between the European wild parsnip Pastinaca sativa and its coevolved florivore the parsnip webworm Depressaria pastinacella, established in North America for over 150 years, has resulted in evolution of local chemical phenotype matching. The recent invasion of New Zealand by webworms, exposing parsnips there to florivore selection for the first time, provided an opportunity to assess rates of adaptive response in a real‐time experiment. We planted reciprocal common gardens in the USA and NZ with seeds from (1) US populations with a long history of webworm association; (2) NZ populations that had never been infested and (3) NZ populations infested for 3 years (since 2007) or 6 years (since 2004). We measured impacts of florivory on realized fitness, reproductive effort and pollination success and measured phenotypic changes in infested NZ populations relative to uninfested NZ populations to determine whether rapid adaptive evolution in response to florivory occurred. Irrespective of country of origin or location, webworms significantly reduced plant fitness. Webworms reduced pollination success in small plants but not in larger plants. Although defence chemistry remained unchanged, plants in infested populations were larger after 3–6 years of webworm florivory. As plant size is a strong predictor of realized fitness, evolution of large size as a component of florivore tolerance may occur more rapidly than evolution of enhanced chemical defence.     

Impact of reassociation with a coevolved herbivore on oviposition deterrence in a hostplant

Although selection by herbivores for increased feeding deterrence in hostplants is well documented, selection for increased oviposition deterrence is rarely examined. We investigated chemical mediation of oviposition by the parsnip webworm (Depressaria pastinacella) on its principal hostplant Pastinaca sativa to determine whether ovipositing adults choose hostplants based on larval suitability and whether hostplants experience selection for increased oviposition deterrence. Webworms consume floral tissues and florivory selects for increased feeding deterrents; moths, however, oviposit on leaves of pre-bolting plants. Exclusive use of different plant parts for oviposition and larval feeding suggests oviposition should select for increased foliar deterrents. Recent webworm colonization of New Zealand (NZ) allowed us to assess phenotypic changes in foliar chemicals in response to webworm oviposition. In a common garden experiment, we compared NZ populations with and without a history of infestation from 2004 to 2006 for changes in leaf chemistry in response to oviposition. Three leaf volatiles, cis- and trans-ocimene, and β-farnesene, elicit strong responses in female moth antennae; these compounds were negatively associated with oviposition and are likely oviposition deterrents. Leaf β-farnesene was positively correlated with floral furanocoumarins that deter florivory; greater oviposition on plants with low floral furanocoumarins indicates that moths preferentially oviposit on parsnips most suitable for larval growth. Unlike florivory, high oviposition on leaves did not lower plant fitness, consistent with the fact that NZ parsnip foliar chemistry was unaffected by 3–6 years of webworm infestation. Thus, in this system, selection by ovipositing moths on foliar chemistry is weaker than selection by larvae on floral chemistry.     

Optimal defence, kin conflict and the distribution of furanocoumarins among offspring of wild parsnip

The factors influencing the allocation of chemical defences to plant offspring have largely been unexplored, conceptually and experimentally. Because evolutionary interactions between maternal plants and their progeny can affect resource allocation patterns among sibling offspring, we suggest that kin conflict as well as herbivore–plant interaction theories need to be considered to predict chemical defence allocation patterns. Optimal defence theory predicts that maternal plants should defend more heavily those offspring in which resources have been disproportionately invested. In contrast, kin conflict theory predicts that natural selection will favour genotypes that can compete successfully for maternal defences irrespective of their quality, even at the expense of the fitness of siblings and the maternal plant. Evidence for these defence patterns were evaluated by examining the allocation of furanocoumarins to seeds of the wild parsnip (Pastinaca sativa, Apiaceae). Furanocoumarins are toxins that are localized within the oil tubes of the maternal tissues of seeds. We evaluated the role of offspring investment (endosperm mass) and seed genotype on furanocoumarin allocation by mating an array of pollen donors with pollen recipients. Furanocoumarins were found to be positively correlated with endosperm mass on one side of the seed, a result consistent with optimal defence theory; however, on the other side of the seed, furanocoumarin content was influenced by seed genotype and was unrelated to endosperm mass. These effects varied with maternal plant. Further experiments demonstrated that nearly 80% of furanocoumarin production occurs after pollination, when fertilization products are active. Although the amount of furanocoumarin influenced by the seed genotype is small relative to the total quantity in the seed, these furanocoumarins are the first line of defence against important predators, such as the parsnip webworm, Depressaria pastinacella (Lepidoptera: Oecophoridae). We found that parsnip webworm larvae were able to discriminate among genotypes within an inflorescence. In line with previous studies, these results suggest that a genotype's ability to influence furanocoumarin defence may affect its probability of survival. We conclude that the distribution of defences among plant offspring in wild parsnip is probably influenced by competition among seed genotypes that conflicts with maternal optimal defence. This revised version was published online in July 2006 with corrections to the Cover Date.     

Effects of florivory on floral volatile emissions and pollination success in the wild parsnip

In addition to reducing fitness by consuming reproductive structures, florivores may also reduce plant fitness by altering interactions with pollinators. To date, the effects of florivore activity on the volatile profile of flowers and subsequent attractiveness to pollinators have not been extensively investigated. In this study, we had three specific objectives: to determine the impact of florivory by the parsnip webworm Depressaria pastinacella on the floral volatile profile of the wild parsnip Pastinaca sativa, to ascertain the mechanisms by which florivory changes the volatile profile, and to estimate the consequences of florivory on visitation by pollinators and eventual seed set. An overall indirect effect of webworms on seed set, that is, the effect of infestation on pollination success, was not detected. However, this overall lack of indirect effect masks the heterogeneity among individual plants. For seven of 14 plants examined, pollination success was altered by webworms, and in four of these plants the alteration in pollination success was consistent with webworm-altered visitation. Webworms significantly altered floral fragrance, in particular causing disproportionate increases in the emissions of octyl esters. Additionally, volatiles from webworm frass, which contains large amounts of the octyl ester metabolite n-octanol, may alter the floral fragrance in ways that change attractiveness of flowers to pollinators. This study suggests that the effects of florivores on plant fitness are not limited to the removal of floral units but may also involve alterations in floral volatile composition, through damage-induced release and detoxification of particular constituents, that affect visitation and pollination success. Handling Editor: Steve Johnson. An erratum to this article can be found at     

Geographic variation in performance of a widespread generalist insect herbivore

1. Generalist herbivores are often widespread and occur in a variety of environments. Due to their broad distribution, it is likely that some populations of generalists will encounter host plants with geographic variation in traits that could affect the herbivore's growth and survival (i.e. performance). However, the geographic pattern of performance has rarely been studied for generalists, especially across large geographic ranges. 2. This study used one of the most generalist herbivore species known, the fall webworm (Hyphantria cunea Drury 1773, Erebidae, Lepidoptera), to experimentally test how the performance of a local population of fall webworms varies with increasing geographic distance of the host plant population from the local herbivore population. Specifically, a transplant experiment was used to compare the performance of one fall webworm population feeding on its local host plants with its performance on host populations from two other locations, 1300 and 2600 km away. 3. It was found that fall webworms performed better on their local host plant populations than on populations from other regions, with performance at its lowest when reared on hosts of the same species from the farthest region. It was also found that local fall webworms do not perform well on hosts commonly used by fall webworms at the other two, more distant sites. 4. This study helps to elucidate how the performance of generalist herbivores varies along their geographic range and suggests possible local adaptation to different sets of hosts across sites.     

Parthenocarpic fruits in wild parsnip: Decoy defence against a specialist herbivore

Summary Parthenocarpy, the production of fruits without viable seeds, is a widespread phenomenon in plants. While failure to effect pollination or fertilization is often cited as the cause of parthenocarpy, this explanation alone is inadequate to explain why plants produce, maintain and further develop fruits. Wild parsnips (Pastinaca sativa) frequently produce parthenocarpic fruit. When parsnip webworms (Depressaria pastinacella), specialist feeders on wild parsnip, were given choices between normal fruit and parthenocarpic fruit, they exhibited a strong preference for parthenocarpic fruit. However, on parthenocarpic fruit, insects fed less efficiently and grew more slowly than insects fed normal fruit. Parthenocarpic fruits, then, may act as decoys that divert herbivores away from fruits that contain plant offspring.     

Extended larval development time for aphid parasitoids in the presence of plant endosymbionts

Abstract 1. Variation in plant chemistry does not only mediate interactions between plants and herbivores but also those between herbivores and their natural enemies, and plants and natural enemies. 2. Endophytic fungi complete their whole life cycle within the host plant’s tissue and are associated with a large diversity of plant species. Endophytes of the genus Neotyphodium alter the chemistry of the host plant by producing herbivore toxic alkaloids. 3. Here we asked whether the endophyte‐tolerant aphid species Metopolophium festucae could be defended against its parasitoid Aphidius ervi when feeding on endophyte‐infected plants. In a laboratory experiment, we compared life‐history traits of A. ervi when exposed to hosts on endophyte‐infected or endophyte‐free Lolium perenne. 4. The presence of endophytes significantly increased larval and pupal development times, but did not affect the mortality of immature parasitoids or the longevity of the adults. Although the number of parasitoid mummies tended to be reduced on endophyte‐infected plants, the number of emerging parasitoids did not differ significantly between the two treatments. 5. This shows that the metabolism of individual aphids feeding on infected plants may be changed and help in the defence against parasitoids. An increase in parasitoid development time should ultimately reduce the population growth of A. ervi. Therefore, endophyte presence may represent an advantage for endophyte‐tolerant aphid species through extended parasitoid development and its effect on parasitoid population dynamics.     

Furanocoumarins in seeds of wild and cultivated parsnip

The furanocoumarin content of ripe seeds of seven cultivars of Pastinaca sativa was compared to that of ripe seeds from a naturalized population in central Illinois. Five furanocoumarins were identified and quantified in the intact seeds. While seeds of wild and cultivated plants contain furanocoumarin components in identical proportions, seeds from wild plants contain almost three times the quantity of furanocoumarins on a dry weight basis as do seeds of cultivars.     

寄主植物-蚜虫-天敌三重营养关系的化学生态学研究进展

综述了寄主植物－蚜虫－天敌三重营养关系的化学生态学研究,重点阐述了3个研究热点：①植物挥发性物质在蚜虫及其天敌选择寄主行为过程中的作用;②蚜虫信息素和蜜露对蚜虫天敌寄主选择行为的影响;③植物挥发性物质对蚜虫信息系作用的影响。对寄主植物－蚜虫－天敌三重营养关系的全面了解,将为蚜虫的综合治疗提供新思维。     

Physiological price of an induced chemical defense: photosynthesis, respiration, biosynthesis, and growth

A recurring theme in defense allocation theories is that defenses are costly. Most studies that attempt to quantify a cost of defense seek to establish a trade-off between a component of plant fitness and the level of a constitutive defense. Such estimates are ambiguous because they cannot discount the cost of traits that are correlated with defense but are not themselves defensive. We examined the effects of damage-induced synthesis of furanocoumarins, known defense compounds, on the growth of wild parsnip. Plants that had 2% of their leaf area removed accumulated 8.6% less total biomass and 14% less root biomass than intact plants over a 4-week period. We also found that this small amount of leaf damage significantly reduced net photosynthetic rates 0.5 h after damage; the effect was temporary, as photosynthetic rates were no longer significantly different after 48 h. Lastly, we found that increases in respiration rates associated with damage coincided spatially and temporally with increases in furanocoumarin production, and that respiration increases were phenotypically correlated with furanocoumarin production. When damage-induced changes in furanocoumarin content and respiration rates were expressed in glucose equivalents and compared, the energetic cost of furanocoumarin production (12.6 μg glucose cm⁻²) accounted for all of the increase in respiration (12.0 μg glucose cm⁻²). A comparison of other secondary compounds in damaged and intact leaflets revealed that myristicin, a furanocoumarin synergist, is the only other compound aside from furanocoumarins that is inducible. The inducible defense system of wild parsnip thus appears to involve a small subset of secondary compounds. Synthesis of these compounds is tightly linked to damage-induced rates of respiration. Because the negative impact that damage had on the rate of net photosynthesis was short-lived, the impact of damage on growth observed in this study was likely due to the cost of furanocoumarin synthesis elicited by damage rather than the loss of photosynthetic tissue caused by damage. Received: 4 April 1996 / Accepted: 29 August 1996     

Dietary specialization and the effects of plant species on potential multitrophic interactions of three species of nymphaline caterpillars

The diet breadth of insect herbivores influences their response to variation in plant quality, and these bitrophic interactions have implications for the higher‐level trophic interactions between herbivores and their natural enemies. In this comparative study, we examined the role of host plant species and plant secondary chemistry on the potential interactions between three species of nymphaline caterpillars and their natural enemies. The caterpillar species (all Lepidoptera: Nymphalidae) varied in their degree of specialization: the buckeye, Junonia coenia Hübner, is a specialist on plants that contain iridoid glycosides (IGs); the white peacock, Anartia jatrophae L., feeds on plants in five families, some of which contain IGs and some of which do not; and the painted lady, Vanessa cardui L., is a generalist, feeding on plants in at least 15 families. Each species was reared on leaves of an introduced host plant, Plantago lanceolata L. (Plantaginaceae), which produces two IGs, aucubin and catalpol, and on another plant species that is a common host plant. These alternate host plants were Plantago major L. (Plantaginaceae) for J. coenia, Bacopa monnieri (L.) Pennell (Plantaginaceae) for A. jatrophae, and Malva parviflora L. (Malvaceae) for V. cardui. We examined growth, sequestration, and immune response of these caterpillars on the different host plant species. Junonia coenia developed more rapidly and sequestered higher IG concentrations when reared on P. lanceolata, whereas both other species grew more slowly on P. lanceolata. Host plant did not influence immune response of J. coenia or A. jatrophae, whereas V. cardui immune response was weaker when reared on P. lanceolata. Junonia coenia was most efficient at IG sequestration and A. jatrophae was least efficient, when all three species were reared on P. lanceolata. These results indicate that diet breadth may play an important role in structuring tritrophic interactions, and this role should be further explored.     

Influence of drought on plant performance through changes in belowground tritrophic interactions

Climate change is predicted to increase the risk of drought in many temperate agroecosystems. While the impact of drought on aboveground plant‐herbivore‐natural enemy interactions has been studied, little is known about its effects on belowground tritrophic interactions and root defense chemistry. We investigated the effects of low soil moisture on the interaction between maize, the western corn rootworm (WCR, Diabrotica virgifera), and soil‐borne natural enemies of WCR. In a manipulative field experiment, reduced soil moisture and WCR attack reduced plant performance and increased benzoxazinoid levels. The negative effects of WCR on cob dry weight and silk emergence were strongest at low moisture levels. Inoculation with entomopathogenic nematodes (EPNs, Heterorhabditis bacteriophora) was ineffective in controlling WCR, and the EPNs died rapidly in the warm and dry soil. However, ants of the species Solenopsis molesta invaded the experiment, were more abundant in WCR‐infested pots and predated WCR independently of soil moisture. Ant presence increased root and shoot biomass and was associated with attenuated moisture‐dependent effects of WCR on maize cob weight. Our study suggests that apart from directly reducing plant performance, drought can also increase the negative effects of root herbivores such as WCR. It furthermore identifies S. molesta as a natural enemy of WCR that can protect maize plants from the negative impact of herbivory under drought stress. Robust herbivore natural enemies may play an important role in buffering the impact of climate change on plant‐herbivore interactions.     

Antagonism between herbivore‐induced plant volatiles and trichomes affects tritrophic interactions

We used tomato genotypes deficient in the jasmonic acid (JA) pathway to study the interaction between the production of herbivore‐induced plant volatiles (HIPVs) that serve as information cues for herbivores as well as natural enemies of herbivores, and the production of foliar trichomes as defence barriers. We found that jasmonic acid‐insensitive1 (jai1) mutant plants with both reduced HIPVs and trichome production received higher oviposition of adult leafminers, which were more likely to be parasitized by the leafminer parasitoids than JA biosynthesis spr2 mutant plants deficient in HIPVs but not trichomes. We also showed that the preference and acceptance of leafminers and parasitoids to trichome‐removed plants from either spr2 or wild‐type (WT) genotypes over trichome‐intact genotypes can be ascribed to the reduced trichomes on treated plants, but not to altered direct and indirect defence traits such as JA, proteinase inhibitor (PI)‐II and HIPVs levels. Although the HIPVs of WT plants were more attractive to adult insects, the insects preferred trichome‐free jai1 plants for oviposition and also had greater reproductive success on these plants. Our results provide strong evidence that antagonism between HIPV emission and trichome production affects tritrophic interactions. The interactions among defence traits are discussed.