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.     

Influence of fungal isolates infecting tall fescue on multitrophic interactions

The epichloae are ascomycetous fungi in the genera Epichloë and Neotyphodium that live within grasses. Some of these fungi produce alkaloids that can help protect the host from herbivores. The alkaloids may also travel up the food web and affect members of the third trophic level. In this way they can produce trophic cascades which are rippling effects when a trophic level impacts those above or below it. We briefly summarize the general patterns of multitrophic effects of endophytes and highlight the most recent studies on this topic. Further, we report on our study in which we tested if different fungal strains in tall fescue (cultivar Jesup) affect multitrophic interactions involving aphids and their parasitoid natural enemies. Using both the common strain of N. coenophialum and a novel isolate (AR577), we allowed potted plants to be colonized by aphids and parasitoids in a semi-natural setting. We found that endophyte infection of tall fescue resulted in greater vegetative growth of the plant. We also found that N. coenophialum modified bottom-up cascades by depressing both aphid and parasitoid densities. Finally, we found that multitrophic effects were modified by fungal isolate: the common strain had stronger negative impacts on aphid and parasitoid densities than did the novel isolate.     

Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection

Complex biotic interactions shape ecological communities of plants, herbivores and their natural enemies. In studies of multi-trophic interactions, the presence of small, invisible micro-organisms associated with plants and those of a fourth above-ground trophic level have often been neglected. Incorporating these neglected factors improves our understanding of the processes within a multi-trophic network. Here, we ask whether the presence of a fungal endosymbiont, which alters plant quality by producing herbivore-toxic substances, trickles up the food chain and affects the performance and host-selection behaviour of aphid secondary parasitoids. We simultaneously offered hosts from endophyte-free and endophyte-infected environments to secondary parasitoids. Older and more experienced parasitoid females discriminated against hosts from the endophyte-infected environment. Developing in lower quality hosts from the endophyte-infected environment reduced the lifespan of secondary parasitoids. This indicates that aphid secondary parasitoids can perceive the disadvantage for their developing offspring in parasitoids from the endophyte environment and can learn to discriminate against them. In the field, this discrimination ability may shift the success of primary parasitoids to endophyte-infected plants, which co-occur with endophyte-free plants. Ultimately, the control of aphids depends on complex interactions between primary and secondary parasitoids and their relative sensitivity to endophytic fungi.     

Effect of belowground herbivory on parasitoid associative learning of plant odours

Root herbivores can influence both the performance and the behaviour of parasitoids of aboveground insect herbivores through changes in aboveground plant quality and in the composition of the plant's odour blend. Here we show that root herbivory by Delia radicum larvae did not influence the innate preferences for plant odours of the two closely related parasitoid species Cotesia glomerata and C. rubecula, but did affect their learned preferences, and did so in an opposite direction. While C. glomerata learned to prefer the odour of plants with intact roots, C. rubecula learned to prefer the odour of root‐infested plants. The learned preference of C. glomerata for the odour of plants with intact roots matches our previously published result of its better performance when developing in P. brassicae hosts feeding on this plant type. In contrast, the relatively stronger learned preference of C. rubecula for the odour of root‐infested plants cannot be merely explained by its performance, as the results of our present study indicate that D. radicum root herbivory did not influence the performance of C. rubecula nor of its host P. rapae. Our results stress the importance of assessing the influence of root herbivores on both innate and learned responses of parasitoids to plant odours.     

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

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

Intra-specific variation in wild Brassica oleracea for aphid-induced plant responses and consequences for caterpillar–parasitoid interactions

Herbivore-induced plant responses not only influence the initiating attackers, but also other herbivores feeding on the same host plant simultaneously or at a different time. Insects belonging to different feeding guilds are known to induce different responses in the host plant. Changes in a plant’s phenotype not only affect its interactions with herbivores but also with organisms higher in the food chain. Previous work has shown that feeding by a phloem-feeding aphid on a cabbage cultivar facilitates the interaction with a chewing herbivore and its endoparasitoid. Here we study genetic variation in a plant’s response to aphid feeding using plants originating from three wild Brassica oleracea populations that are known to differ in constitutive and inducible secondary chemistry. We compared the performance of two different chewing herbivore species, Plutella xylostella and M. brassicae, and their larval endoparasitoids Diadegma semiclausum and M. mediator, respectively, on plants that had been infested with aphids (Brevicoryne brassicae) for 1 week. Remarkably, early infestation with B. brassicae enhanced the performance of the specialist P. xylostella and its parasitoid D. semiclausum, but did not affect that of the generalist M. brassicae, nor its parasitoid M. mediator. Performance of the two herbivore–parasitoid interactions also varied among the cabbage populations and the effect of aphid infestation marginally differed among the three populations. Thus, the effect of aphid infestation on the performance of subsequent attackers is species specific, which may have concomitant consequences for the assembly of insect communities that are naturally associated with these plants.     

Role of foliar fungal endophytes in litter decomposition among species and population origins

Litter decomposition is a key ecosystem process which returns nutrients from dead plant material to mineral forms in the soil. We examined whether systemic fungal endophytes modulate recycling of nutrients directly by altering litter decomposition. We studied litter decomposition mediated by Epichloë endophytes in litter-bag experiments. We examined direct endophyte effects on litter decomposition in wild populations and cultivars of Schedonorus phoenix and Schedonorus pratensis. In the first experiment, endophyte presence tended to increase litter decomposition rate in cultivars of the two grass species (S. phoenix and S. pratensis). However, in the second experiment plant origin had a stronger influence than endophyte symbiosis in S. phoenix. Interestingly, the initial level of alkaloids was associated positively with decomposition in S. phoenix populations. Characteristics associated with litter quality were not clearly related to either endophytes or decomposition rate. Our results suggest that endophytes can enhance litter breakdown but their role in nutrient cycling is far more complex depending on plant population origin.     

Host plant genotype determines bottom‐up effects in an aphid‐parasitoid‐predator system

Plant genotypes are known to affect performance of insect herbivores and the community structure of both herbivores and higher trophic levels. Still, only a limited number of studies demonstrate differences in the performance of predators and parasitoids because of plant genotypic effects and most of these focus on gall formers. We designed a greenhouse experiment to investigate the effects of host plant genotype on fitness components in a grass‐aphid‐carnivore system. We used clones of quackgrass [Elytrigia repens (L.) Desv. ex Nevski (Poaceae)], the aphid Rhopalosiphum padi (L.) (Hemiptera: Aphididae), the parasitoid wasp Aphidius colemani (Viereck) (Hymenoptera: Braconidae), and the predatory lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). The number of aphid offspring differed considerably among plant genotypes. These differences were only in part because of differences in the production of biomass among host genotypes. Therefore, genotypes may differ in their nutritional value for phytophages. The number of aphids attacked by the parasitoid also differed among genotypes and aphid numbers only partly accounted for this effect. Moreover, pupal development time of female parasitoids was affected by plant genotype. We found no differences in mortality, body size, or sex ratio of hatching wasps between genotypes of quackgrass. Development time of the larvae and larval weight of the predatory lacewings differed among genotypes, but not weight of pupae and adults. Generally, the proportion of the total variance explained by the plant genotype was smaller for parasitoids and predators than for aphids. Overall, our experiments indicated that the plant genotype affects tri‐trophic interactions, but also that the strength of these effects decreases along the food chain.     

Plant Quantity Affects Development and Survival of a Gregarious Insect Herbivore and Its Endoparasitoid Wasp

Virtually all studies of plant-herbivore-natural enemy interactions focus on plant quality as the major constraint on development and survival. However, for many gregarious feeding insect herbivores that feed on small or ephemeral plants, the quantity of resources is much more limiting, yet this area has received virtually no attention. Here, in both lab and semi-field experiments using tents containing variably sized clusters of food plants, we studied the effects of periodic food deprivation in a tri-trophic system where quantitative constraints are profoundly important on insect performance. The large cabbage white Pieris brassicae, is a specialist herbivore of relatively small wild brassicaceous plants that grow in variable densities, with black mustard (Brassica nigra) being one of the most important. Larvae of P. brassicae are in turn attacked by a specialist endoparasitoid wasp, Cotesia glomerata. Increasing the length of food deprivation of newly molted final instar caterpillars significantly decreased herbivore and parasitoid survival and biomass, but shortened their development time. Moreover, the ability of caterpillars to recover when provided with food again was correlated with the length of the food deprivation period. In outdoor tents with natural vegetation, we created conditions similar to those faced by P. brassicae in nature by manipulating plant density. Low densities of B. nigra lead to potential starvation of P. brassicae broods and their parasitoids, replicating nutritional conditions of the lab experiments. The ability of both unparasitized and parasitized caterpillars to find corner plants was similar but decreased with central plant density. Survival of both the herbivore and parasitoid increased with plant density and was higher for unparasitized than for parasitized caterpillars. Our results, in comparison with previous studies, reveal that quantitative constraints are far more important that qualitative constraints on the performance of gregarious insect herbivores and their gregarious parasitoids in nature.     

Cascading effects of host size and host plant species on parasitoid resource allocation

1. The bottom‐up factors that determine parasitoid host use are an important area of research in insect ecology. Host size is likely to be a primary cue for foraging parasitoids due to its potential influence on offspring development time, the risk of multiparasitism, and host immunocompetence. Host size is mediated in part by host‐plant traits that influence herbivore growth and potentially affect a herbivore's quality as a host for parasitoids. 2. Here, we tested how caterpillar host size and host plant species influence adult fly parasitoid size and whether host size influences wasp parasitoid sex allocation. We measured the hind tibia lengths and determined the sex of wasp and fly parasitoids reared from 11 common host species of polyphagous caterpillars (Limacodidae) that were in turn reared on foliage of seven different host plant species. 3. We also tested how host caterpillar species, host caterpillar size, and host and parasitoid phenology affect how the parasitoid community partitions host resources. We found evidence that parasitoids primarily partition their shared hosts based on size, but not by host species or phenology. One index of specialisation (d′) supports our observation that these parasitoids are quite generalised within the Limacodidae. In general, wasps were reared from caterpillars collected in early instars, while flies were reared from caterpillars collected in late instars. Furthermore, for at least one species of solitary wasp, host size influenced sex allocation of offspring by ovipositing females. 4. Host‐plant quality indirectly affected the size attained by a tachinid fly parasitoid through its direct effects on the size and performance of the caterpillar host. The host plants that resulted in the highest caterpillar host performance in the absence of enemies also yielded the largest parasitoid flies, which suggests that host plant quality can cascade up to influence the third trophic level.     

The parasitoid of a fruit moth caterpillar utilizes fruit components as nutrient source to increase its longevity and fertility

Longevity and fecundity of female wasps are two decisive factors for the effectiveness of parasitoid species as biological control agents. Accessibility and suitability of nutrient sources determine parasitoid survival and reproduction. Host, nectar and honeydew feeding are frequent adult parasitoid behaviors to cover nutritional needs. Here we postulate that especially parasitoid species of endophytic herbivores might use plant tissue as a nutrient source that becomes accessible upon herbivory. We investigated the influence of plant consumption and host feeding on longevity and fecundity of Hyssopus pallidus, a gregarious ecto-parasitoid of caterpillars of the codling moth that feed inside apple fruits. Longevity of unmated and mated ovipositing female parasitoids was highest in treatments with fruit pulp. While longevity in this treatment was not significantly different from that with honey, it was significantly higher than in treatments without food, with water or with a host alone.Reproduction was significantly increased by these sugar-rich nutrient sources compared to the control with a host alone. In contrast, host feeding did not yield any significant contribution to longevity and fecundity in a series of bioassays with different host–parasitoid ratios and with differently aged and sized hosts, compared to controls without food.We conclude that in this synovigenic species host feeding does not contribute to longevity and fecundity, but females can increase survival and reproduction in the field relying solely on the plant tissue damaged by their host caterpillar.     

The plant hormone salicylic acid interacts with the mechanism of anti‐herbivory conferred by fungal endophytes in grasses

The plant hormone salicylic acid (SA) is recognized as an effective defence against biotrophic pathogens, but its role as regulator of beneficial plant symbionts has received little attention. We studied the relationship between the SA hormone and leaf fungal endophytes on herbivore defences in symbiotic grasses. We hypothesize that the SA exposure suppresses the endophyte reducing the fungal‐produced alkaloids. Because of the role that alkaloids play in anti‐herbivore defences, any reduction in their production should make host plants more susceptible to herbivores. Lolium multiflorum plants symbiotic and nonsymbiotic with the endophyte Epichloë occultans were exposed to SA followed by a challenge with the aphid Rhopalosiphum padi. We measured the level of plant resistance to aphids, and the defences conferred by endophytes and host plants. Symbiotic plants had lower concentrations of SA than did the nonsymbiotic counterparts. Consistent with our prediction, the hormonal treatment reduced the concentration of loline alkaloids (i.e., N‐formyllolines and N‐acetylnorlolines) and consequently decreased the endophyte‐conferred resistance against aphids. Our study highlights the importance of the interaction between the plant immune system and endophytes for the stability of the defensive mutualism. Our results indicate that the SA plays a critical role in regulating the endophyte‐conferred resistance against herbivores.     

Aphid genotypes vary in their response to the presence of fungal endosymbionts in host plants

Genetic variation for fitness‐relevant traits may be maintained in natural populations by fitness differences that depend on environmental conditions. For herbivores, plant quality and variation in chemical plant defences can maintain genetic variation in performance. Apart from plant secondary compounds, symbiosis between plants and endosymbiotic fungi (endophytes) can produce herbivore‐toxic compounds. We show that there is significant variation among aphid genotypes in response to endophytes by comparing life‐history traits of 37 clones of the bird cherry‐oat aphid Rhopalosiphum padi feeding on endophyte‐free and endophyte‐infected tall fescue Lolium arundinaceum. Clonal variation for life‐history traits was large, and most clones performed better on endophyte‐free plants. However, the clones differed in the relative performance across the two environments, resulting in significant genotype × environment interactions for all reproductive traits. These findings suggest that natural variation in prevalence of endophyte infection can contribute to the maintenance of genetic diversity in aphid populations.     

A tritrophic approach to the preference–performance hypothesis involving an exotic and a native plant

Exotic plants often generate physical and chemical changes in native plant communities where they become established. A major challenge is to understand how novel plants may affect trophic interactions in their new habitats, and how native herbivores and their natural enemies might respond to them. We compared the oviposition preference and offspring performance of the crucifer specialist, Pieris brassicae, on an exotic plant, Bunias orientalis, and on a related native plant, Sinapis arvensis. Additionally, we studied the response of the parasitoid, Cotesia glomerata to herbivore-induced plant volatiles (HIPV) and determined the volatile blend composition to elucidate which compound(s) might be involved in parasitoid attraction. On both host plants we also compared the parasitism rate of P. brassicae by C. glomerata. Female butterflies preferred to oviposit on the native plant and their offspring survival and performance was higher on the native plant compared to the exotic. Although, headspace analysis revealed qualitative and quantitative differences in the volatile blends of both plant species, C. glomerata did not discriminate between the HIPV blends in flight-tent bioassays. Nevertheless, parasitism rate of P. brassicae larvae was higher on the native plant under semi-field conditions. Overall, P. brassicae oviposition preference may be more influenced by bottom-up effects of the host plant on larval performance than by top-down pressure exerted by its parasitoid. The potential for dietary breadth expansion of P. brassicae to include the exotic B. orientalis and the role of top-down processes played by parasitoids in shaping herbivore host shifts are further discussed.     

Cascading effects of variation in plant vigour on the relative performance of insect herbivores and their parasitoids

Abstract 1. Consequences of variation in food plant quality were estimated for a system consisting of two monophagous noctuid herbivores and three ichneumonid parasitoids.
2. In a natural population, pupal weights of the herbivores in this system, Nonagria typhae and Archanara sparganii , were found to be highly variable. Pupal weights increased strongly and consistently with the increase in the vigour of the host plant, Typha latifolia , providing support for the plant vigour hypothesis. Correspondingly, as the moths do not feed as adults, a strong, positive correlation between host vigour and fecundity of the herbivores would be expected.
3. There were strong and positive relationships between adult body sizes of the parasitoids and the sizes of their lepidopteran hosts. Moreover, a direct, positive link between plant quality and parasitoid size was documented.
4. For all three parasitoids, cascading effects of plant quality on body size were weaker than for the herbivores. Differences in the importance of adult feeding and oviposition behaviour suggest that dependence of fitness on body size is also weaker in the parasitoids than in the moths. It is therefore concluded that the numerical response of the herbivore population to a change in plant quality should exceed the corresponding response in the parasitoids.
5. The results of this work imply that variation in plant variables may affect performance of different trophic levels to a different extent. It is suggested that the importance of adult feeding for the reproductive success (capital vs. income breeding strategies) in both herbivores and parasitoids is an essential aspect to consider when predicting responses of such a system to changes in plant quality.     

Indirect plant-mediated interactions among parasitoid larvae

Communities are riddled with indirect species interactions and these interactions can be modified by organisms that are parasitic or symbiotic with one of the indirectly interacting species. By inducing plant responses, herbivores are well known to alter the plant quality for subsequent feeders. The reduced performance of herbivores on induced plants cascades into effects on the performance of higher trophic level organisms such as parasitoids that develop inside herbivores. Parasitoids themselves may also, indirectly, interact with the host plant by affecting the behaviour and physiology of their herbivorous host. Here, we show that, through their herbivorous host, larvae of two parasitoid species differentially affect plant phenotypes leading to asymmetric interactions among parasitoid larvae developing in different hosts that feed on the same plant. Our results show that temporally separated parasitoid larvae are involved in indirect plant-mediated interactions by a network of trophic and non-trophic relationships.     

Habitats as Complex Odour Environments: How Does Plant Diversity Affect Herbivore and Parasitoid Orientation?

Plant diversity is known to affect success of host location by pest insects, but its effect on olfactory orientation of non-pest insect species has hardly been addressed. First, we tested in laboratory experiments the hypothesis that non-host plants, which increase odour complexity in habitats, affect the host location ability of herbivores and parasitoids. Furthermore, we recorded field data of plant diversity in addition to herbivore and parasitoid abundance at 77 grassland sites in three different regions in Germany in order to elucidate whether our laboratory results reflect the field situation. As a model system we used the herb Plantago lanceolata, the herbivorous weevil Mecinus pascuorum, and its larval parasitoid Mesopolobus incultus. The laboratory bioassays revealed that both the herbivorous weevil and its larval parasitoid can locate their host plant and host via olfactory cues even in the presence of non-host odour. In a newly established two-circle olfactometer, the weeviĺs capability to detect host plant odour was not affected by odours from non-host plants. However, addition of non-host plant odours to host plant odour enhanced the weeviĺs foraging activity. The parasitoid was attracted by a combination of host plant and host volatiles in both the absence and presence of non-host plant volatiles in a Y-tube olfactometer. In dual choice tests the parasitoid preferred the blend of host plant and host volatiles over its combination with non-host plant volatiles. In the field, no indication was found that high plant diversity disturbs host (plant) location by the weevil and its parasitoid. In contrast, plant diversity was positively correlated with weevil abundance, whereas parasitoid abundance was independent of plant diversity. Therefore, we conclude that weevils and parasitoids showed the sensory capacity to successfully cope with complex vegetation odours when searching for hosts.     

Effects of genetic diversity of grass on insect species diversity at higher trophic levels are not due to cascading diversity effects

Genetic diversity in plant populations has been shown to affect the species diversity of insects. In grasses, infection with fungal endophytes can also have strong effects on insects, potentially modifying the effects of plant genetic diversity. We manipulated the genetic diversity and endophyte infection of a grass in a field experiment. We show that diversity of primary parasitoids (3rd trophic level) and, especially, secondary parasitoids (4th trophic level) increases with grass genetic diversity while there was no effect of endophyte infection. The increase in insect diversity appeared to be due to a complementarity effect rather than a sampling effect. The higher parasitoid diversity could not be explained by a cascading diversity effect because herbivore diversity was not affected and the same herbivore species were present in all treatments. The effects on the higher trophic levels must therefore be due to a direct response to plant traits or mediated by effects on traits at intermediate trophic levels.     

Population genetic structure of two primary parasitoids of Spodoptera frugiperda (Lepidoptera), Chelonus insularis and Campoletis sonorensis (Hymenoptera): to what extent is the host plant important?

Plant chemistry can strongly influence interactions between herbivores and their natural enemies, either by providing volatile compounds that serve as foraging cues for parasitoids or predators, or by affecting the quality of herbivores as hosts or prey. Through these effects plants may influence parasitoid population genetic structure. We tested for a possible specialization on specific crop plants in Chelonus insularis and Campoletis sonorensis, two primary parasitoids of the fall armyworm, Spodoptera frugiperda. Throughout Mexico, S. frugiperda larvae were collected from their main host plants, maize and sorghum and parasitoids that emerged from the larvae were used for subsequent comparison by molecular analysis. Genetic variation at eight and 11 microsatellites were respectively assayed for C. insularis and C. sonorensis to examine isolation by distance, host plant and regional effects. Kinship analyses were also performed to assess female migration among host‐plants. The analyses showed considerable within population variation and revealed a significant regional effect. No effect of host plant on population structure of either of the two parasitoid species was found. Isolation by distance was observed at the individual level, but not at the population level. Kinship analyses revealed significantly more genetically related—or kin—individuals on the same plant species than on different plant species, suggesting that locally, mothers preferentially stay on the same plant species. Although the standard population genetics parameters showed no effect of plant species on population structure, the kinship analyses revealed that mothers exhibit plant species fidelity, which may speed up divergence if adaptation were to occur.     

Effects of glucosinolates on a generalist and specialist leaf-chewing herbivore and an associated parasitoid

Glucosinolates (GLS) are secondary plant metabolites that as a result of tissue damage, for example due to herbivory, are hydrolysed into toxic compounds that negatively affect generalist herbivores. Specialist herbivores have evolved specific adaptations to detoxify GLS or inhibit the formation of toxic hydrolytic products. Although rarely studied, GLS and their breakdown products may also affect parasitoids. The objectives were to test the effects of GLS in a multitrophic system consisting of the generalist herbivore Spodoptera exigua, the specialist herbivore Pieris rapae, and the endoparasitoid Hyposoter ebeninus. Three ecotypes of Arabidopsis thaliana that differ in their GLS composition and concentrations and one transformed line that constitutively produces higher concentrations of aliphatic GLS were used, the latter allowing a direct assessment of the effects of aliphatic GLS on insect performance.Feeding by the generalist S. exigua and the specialist P. rapae induced both higher aliphatic and indole GLS concentrations in the A. thaliana ecotypes, although induction was stronger for indole than aliphatic GLS. For both herbivores a negative correlation between performance and aliphatic GLS concentrations was observed. This suggests that the specialist, despite containing a nitrile-specifier protein (NSP) that diverts GLS degradation from toxic isothiocyanates to less toxic nitriles, cannot completely inhibit the formation of toxic GLS hydrolytic products, or that the costs of this mechanism are higher at higher GLS concentrations. Surprisingly, performance of the parasitoid was positively correlated with higher concentrations of aliphatic GLS in the plant, possibly caused by negative effects on host immune responses. Our study indicates that GLS can not only confer resistance against herbivores directly, but also indirectly by increasing the performance of the parasitoids of these herbivores.