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Upon parasitism, many parasitoids inject symbiotic viruses and venom into their host. Thereby, they modify the hosts physiology including its saliva composition and, in turn, plant perception of herbivory. It has been hypothesised that parasitoids manipulate plant responses to increase their host performance and maximise their own fitness. However, it is still unclear whether parasitoids are under selective pressure to increase plant quality or whether indirect changes in plants due to parasitism are a by-product of the physiological changes induced in their host. We tested whether the parasitoids Hyposoter ebeninus and Cotesia glomerata manipulate induced plant responses through the host Pieris brassicae caterpillars to increase their own performance. During their entire lifespan, parasitised herbivores were fed with leaf material of Brassica oleracea plants that were left untreated or continuously exposed to feeding by either unparasitised, conspecific or heterospecific parasitised caterpillars. We measured the development time, weight, clutch size and mortality of parasitoids that emerged from caterpillars as proxy for their performance. Both parasitoid species did not perform significantly better when their host was fed with leaves from plants continuously induced by a conspecific parasitoid relative to unparasitised caterpillars. However, parasitoid species asymmetrically affected each other's performance through plant-mediated interactions. Our results do not support the hypothesis of parasitoids manipulating plant responses for their own benefit, suggesting that indirect plant-mediated interactions among parasitoids may be a by-product of host manipulation. However, our work confirms the significance of parasitoid-induced plant-mediated interactions in insect communities that to date are still understudied.

Tritrophic interactions among plants, herbivorous insects and their parasitoids have been well studied in the past four decades. Recently, a new angle has been uncovered: koinobiont parasitoids, that allow their host to keep feeding on the plant for a certain amount of time after parasitism, indirectly alter plant responses against herbivory via the many physiological changes induced in their herbivorous hosts. By affecting plant responses, parasitoids may indirectly affect the whole community of insects interacting with plants induced by parasitized herbivores and have extended effects on plant fitness. These important findings have renewed research interests on parasitoid manipulation of their host development. Parasitoids typically arrest their host development before the last instar, resulting in a lower final weight compared to unparasitized hosts. Yet, some parasitoids prolong their host development, leading to larger herbivores that consume more plant material than unparasitized ones. Furthermore, parasitoid host regulation is plastic and one parasitoid species may arrest or promote its host growth depending on the number of eggs laid, host developmental stage and species as well as environmental conditions. The consequences of plasticity in parasitoid host regulation for plant–insect interactions have received very little attention over the last two decades, particularly concerning parasitoids that promote their host growth. In this review, we first synthesize the mechanisms used by parasitoids to regulate host growth and food consumption. Then, we identify the evolutionary and environmental factors that influence the direction of parasitoid host regulation in terms of arrestment or promotion of host growth. In addition, we discuss the implication of different host regulation types for the parasitoid’s role as agent of plant indirect defence. Finally, we argue that the recent research interests about parasitoid plant-mediated interactions would strongly benefit from revival of research on the mechanisms, ecology and evolution of host regulation in parasitoids.

Generalist predators are increasingly used in biological pest control for greenhouse crops, as they control multiple pests and persist in crops even when prey is scarce. However, some of these predators may cause plant damage due to their omnivorous feeding behaviour. In many European regions, the omnivorous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is considered to be a serious tomato pest, regardless of the biological control services it offers, and integrated pest management (IPM) strategies are based instead on Macrolophus pygmaeus (Rambur). However, as N. tenuis may competitively displace M. pygmaeus and cause severe damage, growers often resort to pesticide use, disrupting their biological control practice. In this study, we evaluated the competitive interactions of three mirid predators, Dicyphus errans Wolff, Dicyphus bolivari Lindberg, and Dicyphus cerastii Wagner, with N. tenuis. The results showed that pre-establishment of heterospecific mirid species can successfully suppress N. tenuis in the greenhouse; population growth was reduced by more than 90% compared to plants without competing predators. Further laboratory trials revealed reciprocal intraguild predation between these species in the absence of extraguild prey. Dicyphus adults predated on N. tenuis nymphs, while this was not found for M. pygmaeus. In olfactometer bioassays, N. tenuis females preferred plants previously exposed to heterospecifics but not conspecifics, suggesting that this mirid does not avoid competition. These results suggest that the three Dicyphus species could be interesting candidates for preventive releases in tomato crops due to their ability to effectively suppress N. tenuis population growth.

Insect herbivores interact via plant-mediated interactions in which one herbivore species induces changes in plant quality that affects the performance of a second phytophagous insect that shares the food plant. These interactions are often asymmetric due to specificity in induced plant responses to herbivore attack, amount of plant damage, elicitors in herbivore saliva and plant organ damaged by herbivores. Parasitoids and their symbiotic polydnaviruses alter herbivore physiology and behaviour and may influence how plants respond to parasitized herbivores. We argue that these phenomena affect plant-mediated interactions between herbivores. We identify that the extended phenotype of parasitoid polydnaviruses is an important knowledge gap in interaction networks of insect communities.

The phenotypic plasticity of flowering plants in response to herbivore damage to vegetative tissues can affect plant interactions with flower-feeding organisms. Such induced systemic responses are probably regulated by defence-related phytohormones that signal flowers to alter secondary chemistry that affects resistance to florivores. Current knowledge on the effects of damage to vegetative tissues on plant interactions with florivores and the underlying mechanisms is limited. We compared the preference and performance of two florivores on flowering Brassica nigra plants damaged by one of three herbivores feeding from roots or leaves. To investigate the underlying mechanisms, we quantified expression patterns of marker genes for defence-related phytohormonal pathways, and concentrations of phytohormones and glucosinolates in buds and flowers. Florivores displayed contrasting preferences for plants damaged by herbivores feeding on roots and leaves. Chewing florivores performed better on plants damaged by folivores, but worse on plants damaged by the root herbivore. Chewing root and foliar herbivory led to specific induced changes in the phytohormone profile of buds and flowers. This resulted in increased glucosinolate concentrations for leaf-damaged plants, and decreased glucosinolate concentrations for root-damaged plants. The outcome of herbivore–herbivore interactions spanning from vegetative tissues to floral tissues is unique for the inducing root/leaf herbivore and receiving florivore combination.

Parasitoids need to find their hosts in patchy environments that differ in profitability. To maximize foraging efficiency, parasitoids use volatile information of plants on which their hosts feed. The blend of plant volatiles emitted is affected by genetic variation in plants and by the herbivore species feeding on the plant. How parasitoids deal with variation in plant volatiles induced by host or nonhost herbivores on various plant genotypes in a plant stand is unclear. In a wind tunnel, we examined foraging behaviour of the parasitoid Cotesia glomerata in mixes of white cabbage cultivars with host (Pieris brassicae) and nonhost herbivores (Mamestra brassicae or Delia radicum). We specifically studied the efficiency of parasitoids in locating a host-infested plant when having to pass three other plants that varied in volatile emission by cultivar and herbivore identity. We show that foraging decisions of C. glomerata are affected by the apparency of volatile cues from upwind host-infested plants. We found that parasitoids flew over the first three plants more often when the last plant was a host-infested attractive cultivar and the first three plants were a less attractive cultivar, regardless of the presence of host or nonhost herbivores. Furthermore, parasitoids spent more time on the first three plants if these were infested with host or nonhost larvae, and this effect was stronger when the first three plants were of the attractive cultivar. Our results suggest that parasitoids may more easily locate host herbivores on plant genotypes with more apparent volatile information. However, host location efficiency is affected by the contrast with other plumes of plant volatiles derived from genotypic variation in plants and induction of volatiles by nonhost herbivores. Apparency of information on upwind patches influences patch residence time and patch choice and is an important component of optimal foraging in parasitoids.

Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of their caterpillar host, affecting organismal odours and interactions with insects of higher trophic levels such as hyperparasitoids. Hyperparasitoids parasitise larvae or pupae of parasitoids, which are often concealed or inconspicuous. Odours of parasitised caterpillars aid them to locate their host, but the origin of these odours and its relationship to the caterpillar microbiome are unknown. Here, we analysed the odours and microbiome of the large cabbage white caterpillar Pieris brassicae in relation to parasitism by its endoparasitoid Cotesia glomerata. We identified how bacterial presence in and on the caterpillars is correlated with caterpillar odours and tested the attractiveness of parasitised and unparasitised caterpillars to the hyperparasitoid Baryscapus galactopus. We manipulated the presence of the external microbiome and the transient internal microbiome of caterpillars to identify the microbial origin of odours. We found that parasitism by C. glomerata led to the production of five characteristic volatile products and significantly affected the internal and external microbiome of the caterpillar, which were both found to have a significant correlation with caterpillar odours. The preference of the hyperparasitoid was correlated with the presence of the external microbiome. Likely, the changes in external microbiome and body odour after parasitism were driven by the resident internal microbiome of caterpillars, where the bacterium Wolbachia sp. was only present after parasitism. Micro-injection of Wolbachia in unparasitised caterpillars increased hyperparasitoid attraction to the caterpillars compared to untreated caterpillars, while no differences were found compared to parasitised caterpillars. In conclusion, our results indicate that host-parasite interactions can affect multi-trophic interactions and hyperparasitoid olfaction through alterations of the microbiome.

Root herbivores pose a major threat to agricultural crops. They are difficult to control and their damage often goes unnoticed until the larvae reach their most devastating late instar stages. Crop diversification can reduce pest pressure, generally without compromising yield. We studied how different diversified cropping systems affected the oviposition and abundance of the specialist cabbage root fly Delia radicum, the most important root herbivore in Brassica crops. The cropping systems included a monoculture, pixel cropping, and four variations of strip cropping with varying intra- and interspecific crop diversity, fertilization and spatial configuration. Furthermore, we assessed whether there was a link between D. radicum and other macroinvertebrates associated with the same plants. Cabbage root fly oviposition was higher in strip cropping designs compared to the monoculture and was highest in the most diversified strip cropping design. Despite the large number of eggs, there were no consistent differences in the number of larvae and pupae between the cropping systems, indicative of high mortality of D. radicum eggs and early instars especially in the strip cropping designs. D. radicum larval and pupal abundance positively correlated with soil-dwelling predators and detritivores and negatively correlated with other belowground herbivores. We found no correlations between the presence of aboveground insect herbivores and the number of D. radicum on the roots. Our findings indicate that root herbivore presence is determined by a complex interplay of many factors, spatial configuration of host plants, and other organisms residing near the roots.

In response to herbivory, most plant species adjust their chemical and morphological phenotype to acquire induced resistance to the attacking herbivore. Induced resistance may be an optimal defence strategy that allows plants to reduce metabolic costs of resistance in the absence of herbivores, allocate resistance to the most valuable plant tissues and tailor its response to the pattern of attack by multiple herbivore species. Moreover, plasticity in resistance decreases the potential that herbivores adapt to specific plant resistance traits and need to deal with a moving target of variable plant quality. Induced resistance additionally allows plants to provide information to other community members to attract natural enemies of its herbivore attacker or inform related neighbouring plants of pending herbivore attack. Despite the clear evolutionary benefits of induced resistance in plants, crop protection strategies to herbivore pests have not exploited the full potential of induced resistance for agriculture. Here, we present evidence that induced resistance offers strong potential to enhance resistance and resilience of crops to (multi-) herbivore attack. Specifically, induced resistance promotes plant plasticity to cope with multiple herbivore species by plasticity in growth and resistance, maximizes biological control by attracting natural enemies and, enhances associational resistance of the plant stand in favour of yield. Induced resistance may be further harnessed by soil quality, microbial communities and associational resistance offered by crop mixtures. In the transition to more sustainable ecology-based cropping systems that have strongly reduced pesticide and fertilizer input, induced resistance may prove to be an invaluable trait in breeding for crop resilience.

In nature, plants interact with multiple insect herbivores that may arrive simultaneously or sequentially. There is extensive knowledge on how plants defend themselves against single or dual attack. However, we lack information on how plants defend against the attack of multiple herbivores that arrive sequentially. In this study, we investigated whether Brassica nigra L. plants are able to defend themselves against caterpillars of the late-arriving herbivore Plutella xylostella L., when plants had been previously exposed to sequential attack by four other herbivores (P. xylostella, Athalia rosae, Myzus persicae and Brevicoryne brassicae). We manipulated the order of arrival and the history of attack by four herbivores to investigate which patterns in sequential herbivory determine resistance against the fifth attacker. We recorded that history of sequential herbivore attack differentially affected the capability of B. nigra plants to defend themselves against caterpillars of P. xylostella. Caterpillars gained less weight on plants attacked by a sequence of four episodes of attack by P. xylostella compared to performance on plants that were not previously damaged by herbivores. The number of times the plant was attacked by herbivores of the same feeding guild, the identity of the first attacker, the identity and the guild of the last attacker as well as the order of attackers within the sequence of multiple herbivores influenced the growth of the subsequent herbivory. In conclusion, this study shows that history of sequential attack is an important factor determining plant resistance to herbivores.

Insect herbivores can directly affect plant reproduction by feeding on reproductive tissues, or indirectly by feeding on vegetative tissues for which plants are unable to compensate. Additionally, early arriving herbivores may have cascading effects on plant fitness by altering the richness and abundance of the later arriving community.Studies are divided on whether herbivory early in the development of plants can impact plant fitness and whether these effects are predominantly mediated through changes in plant development or subsequent herbivory. Obtaining insight into the generality and consistency of mediated effects on plant reproduction induced by early-season herbivory requires a comparative approach across plant species and environmental conditions.By excluding the herbivore community in an exclosure experiment and by manipulating early-season herbivory in a common garden experiment replicated across four Brassicaceae species and two years, we tested whether early-season herbivory could affect plant development, reproduction, and the herbivore communities associated with individual plants. In addition, we tested a causal hypothesis to disentangle the direct effect of herbivory on plant reproduction, and their indirect effect through changes in the development of plants.Early-season herbivory affected plant development and reproduction, but effects were highly dependent on the plant species, the inducing herbivore species, and the biotic and abiotic environment. The exploratory path analysis indicated that plant reproduction was best predicted by variation in plant development, explaining up to 90.88% of the total effect on seed production. Even though the richness and abundance of the subsequent herbivore community were conditionally affected by the initial colonising herbivore, herbivore pressure is predicted to have only minor effects on reproduction. Importantly, the effects of herbivore pressure on seed set were not direct but were mediated by changes in plant development.Synthesis:Early-season herbivory has the potential to affect plant reproduction through changes in the development of plants and, less strongly, through effects mediated by the plant-associated herbivore community. However, as plants are often able to compensate and attenuate the effects induced by herbivory, the detection, sign, and strength of effects are highly dependent on the plant species and environment.

Koinobiont parasitoids induce physiological changes in their herbivorous hosts that affect how plants respond to herbivory. The signature of parasitoids on induced plant responses to feeding by parasitized herbivores indirectly impacts insect communities interacting with the plant. The effect may extend to parasitoids and cause indirect interaction between parasitoids that develop inside different herbivore hosts sharing the food plant. However, this type of indirect plant-mediated interactions (IPMIs) among parasitoid larvae has received very little attention. In this study, we investigated sequential and simultaneous plant-mediated interactions among two host-parasitoid systems feeding on Brassica oleracea plants: Mamestra brassicae parasitized by Microplitis mediator and Pieris rapae parasitized by Cotesia rubecula. We measured the mortality, development time and weight of unparasitized herbivores and performance of parasitoids that had developed inside the two herbivore species when sharing the food plant either simultaneously or sequentially. Plant induction by parasitized or unparasitized hosts had no significant effect on the performance of the two herbivore host species. In contrast, the two parasitoid species had asymmetrical indirect plant-mediated effects on each other’s performance. Cotesia rubecula dry weight was significantly increased by plants induced by M. mediator-parasitized hosts, while M. mediator development time was reduced by plant induced responses to conspecific but not to heterospecific parasitoids. Contrary to sequential feeding, parasitoids had no effect on each others performance when feeding simultaneously. These results reveal that indirect plant-mediated interactions among parasitoid larvae could involve any parasitoid species whose hosts share a food plant.

Plants have evolved plastic defence strategies to deal with the uncertainty of when, by which species and in which order attack by herbivores will take place1–3. However, the responses to current herbivore attack may come with a cost of compromising resistance to other, later arriving herbivores. Due to antagonistic cross-talk between physiological regulation of plant resistance to phloem-feeding and leaf-chewing herbivores4–8, the feeding guild of the initial herbivore is considered to be the primary factor determining whether resistance to subsequent attack is compromised. We show that, by investigating 90 pairwise insect–herbivore interactions among ten different herbivore species, resistance of the annual plant Brassica nigra to a later arriving herbivore species is not explained by feeding guild of the initial attacker. Instead, the prevalence of herbivore species that arrive on induced plants as approximated by three years of season-long insect community assessments in the field explained cross-resistance. Plants maintained resistance to prevalent herbivores in common patterns of herbivore arrival and compromises in resistance especially occurred for rare patterns of herbivore attack. We conclude that plants tailor induced defence strategies to deal with common patterns of sequential herbivore attack and anticipate arrival of the most prevalent herbivores. Plants have developed defences against herbivores, but with multiple threats at different times, those defences may be compromised. This experiment finds that plants adapt over time to anticipate prevalent herbivores and common patterns of attack.

Species-specific responses to the environment can moderate the strength of interactions between plants, herbivores and parasitoids. However, the ways in which characteristics of plants, such as genotypic variation in herbivore induced volatiles (HIPVs) that attract parasitoids, affect trophic interactions in different contexts of plant patch size and plant neighbourhood is not well understood. We conducted a factorial field experiment with white cabbage Brassica oleracea accessions that differ in the attractiveness of their HIPVs for parasitoids, in the context of different patch sizes and presence or absence of surrounding Brassica nigra plants. Parasitism rates of experimentally introduced Pieris brassicae caterpillars and the presence of naturally occurring Pieris spp. caterpillars in the plots were assessed throughout the growing season. The abundance of Pieris caterpillars was neither affected by cabbage accession nor plot size. Later in the season, when B. nigra plants had senesced, fewer caterpillars were found on cabbage plants in plots with a B. nigra border. Parasitism rates fluctuated over the season, and were not affected by plot size. However, the B. nigra border negatively affected parasitism rates on the accession that is less attractive to the parasitoid Cotesia glomerata, but not on the more attractive accession. Our results show that plant variation in HIPVs can differentially influence herbivores and parasitoids depending on characteristics of the surrounding vegetation context. These findings underscore the importance of considering the interaction between focal plant traits and neighbourhood context to reliably predict trophic cascades.

Plants show ontogenetic variation in growth–defence strategies to maximize reproductive output within a community context. Most work on plant ontogenetic variation in growth–defence trade‐offs has focussed on interactions with antagonistic insect herbivores. Plants respond to herbivore attack with phenotypic changes. Despite the knowledge that plant responses to herbivory affect plant mutualistic interactions with pollinators required for reproduction, indirect interactions between herbivores and pollinators have not been included in the evaluation of how ontogenetic growth–defence trajectories affect plant fitness.In a common garden experiment with the annual Brassica nigra, we investigated whether exposure to various herbivore species on different plant ontogenetic stages (vegetative, bud or flowering stage) affects plant flowering traits, interactions with flower visitors and results in fitness consequences for the plant.Effects of herbivory on flowering plant traits and interactions with flower visitors depended on plant ontogeny. Plant exposure in the vegetative stage to the caterpillar Pieris brassicae and aphid Brevicoryne brassicae led to reduced flowering time and flower production, and resulted in reduced pollinator attraction, pollen beetle colonization, total seed production and seed weight. When plants had buds, infestation by most herbivore species tested reduced flower production and pollen beetle colonization. Pollinator attraction was either increased or reduced. Plants infested in the flowering stage with P. brassicae or Lipaphis erysimi flowered longer, while infestation by any of the herbivore species tested increased the number of flower visits by pollinators.Our results show that the outcome of herbivore–flower visitor interactions in B. nigra is specific for the combination of herbivore species and plant ontogenetic stage. Consequences of herbivory for flowering traits and reproductive output were strongest when plants were attacked early in life. Such differences in selection pressures imposed by herbivores to specific plant ontogenetic stages may drive the evolution of distinct ontogenetic trajectories in growth–defence–reproduction strategies and include indirect interactions between herbivores and flower visitors. Synthesis. Plant ontogeny can define the direct and indirect consequences of herbivory. Our study shows that the ontogenetic stage of plant individuals determined the effects of herbivory on plant flowering traits, interactions with flower visitors and plant fitness., Plants show ontogenetic variation in growth–defence strategies to maximize reproductive output within a community context. Our study shows that the ontogenetic stage of plant individuals determined the effects of herbivory on plant flowering traits, interactions with flower visitors and plant fitness. Hence, studies on plant evolution need to consider ecologically relevant timing of herbivory.

Parasitoids need to find their plant-feeding hosts in complex environments that contain multiple other plant and insect species. They usually rely on herbivore-induced plant volatiles to locate herbivore-infested plants from a distance and their foraging efficiency may be reduced when volatile information is not available. Downwind foraging during times when high wind speeds prevent odour-guided upwind flights may create foraging situations with limited accessibiliy to volatile information. We hypothesized that parasitoids forage less efficiently by landing on nonhost-damaged or undamaged plants when they are forced to fly downwind and tested this in a wind tunnel experiment. We released the parasitoid Cotesia glomerata (Hymenoptera, Braconidae) either upwind or downwind of a plant stand and observed their foraging behaviour. During downwind foraging, parasitoids were less successful in host finding and needed more time until they managed to oviposit in a host caterpillar compared to the upwind foraging situation. The observed increase in foraging time was caused by prolonged foraging on nonhost-infested and undamaged plants in the downwind situation, indicating that parasitoids leave an unprofitable patch that does not contain host caterpillars earlier, when they perceive volatiles from other herbivore-infested plants located upwind. Volatile information on the availability of herbivore-infested plants within a plant stand seems to be crucial for efficient foraging in plant stands that contain a mixture of host-infested, nonhost-infested and undamaged plants. Parasitoid foraging efficiency may thus be strongly reduced when high wind speed prevents odour-guided upwind flight.

Context Tritrophic interactions may be affected by local factors and the broader landscape context. At small spatial scales, carnivorous enemies of herbivorous insects use herbivore-induced plant volatiles (HIPVs) to find herbivores, but it is unknown whether variation in plant attractiveness due to differential HIPV emission can enhance recruitment of carnivores from the wider landscape. Objectives We studied whether parasitism of caterpillars of the butterfly Pieris brassicae on white cabbage was influenced by landscape composition and cover with brassicaceous species that provide hosts for parasitoids of P. brassicae in 19 landscapes in the Netherlands. We also investigated whether differential attraction of parasitoids to herbivore-infested plants affected parasitism of P. brassicae caterpillars by using different accessions as proxies for HIPV emission. Results The cabbage accession that is highly attractive to parasitic wasps recruited more wasps than a less attractive accession, but only when parasitism rates were high. Parasitism rate as proxy of wasp recruitment correlated positively with the cover of brassicaceous plants and area of arable land, suggesting that these habitats support hosts for the wasps and their population growth. In contrast, forest area was negatively associated with parasitism rates. Conclusions Our study shows that the degree of attractiveness of plants to parasitoids, which is probably mediated by HIPVs, can be a useful predictor of parasitism, but needs to be considered within the landscape context. To understand the strength of tritrophic interactions it is crucial to consider local-scale processes driven by plant-trait variation in combination with landscape-scale processes that determine carnivore abundance.

Polyphagous insects often show specialization in feeding on different host plants in terms of survival and growth and, therefore, can be considered minor or major pests of particular hosts. Whether polyphagous insects employ a common transcriptional response to cope with defenses from diverse host plants is under-studied. We focused on patterns of transcriptional plasticity in polyphagous moths (Noctuidae), of which many species are notorious pests, in relation to herbivore performance on different host plants. We compared the transcriptional plasticity of five polyphagous moth species feeding and developing on three different host plant species. Using a comparative phylogenetic framework, we evaluated if successful herbivory, as measured by larval performance, is determined by a shared or lineage-specific transcriptional response. The upregulated transcriptional activity, or gene expression pattern, of larvae feeding on the different host plants and artificial control diet was highly plastic and moth species-specific. Specialization, defined as high herbivore success for specific host plants, was not generally linked to a lower number of induced genes. Moths that were more distantly related and showing high herbivore success for certain host plants showed shared expression of multiple homologous genes, indicating convergence. We further observed specific transcriptional responses within phylogenetic lineages. These expression patterns for specific host plant species are likely caused by shared evolutionary histories, for example, symplesiomorphic patterns, and could therefore not be associated with herbivore success alone. Multiple gene families, with roles in plant digestion and detoxification, were widely expressed in response to host plant feeding but again showed highly moth species-specific. Consequently, high herbivore success for specific host plants is also driven by species-specific transcriptional plasticity. Thus, potential pest moths display a complex and species-specific transcriptional plasticity.

Hyperparasitoids are some of the most diverse members of insect food webs. True hyperparasitoids parasitize the larvae of other parasitoids, reaching these larvae with their ovipositor through the herbivore that hosts the parasitoid larva. During pupation, primary parasitoids also may be attacked by pseudohyperparasitoids that lay their eggs on the parasitoid (pre)pupae. By attacking primary parasitoids, hyperparasitoids may affect herbivore population dynamics, and they have been identified as a major challenge in biological control. Over the past decades, research, especially on aphid- and caterpillar-associated hyperparasitoids, has revealed that hyperparasitoids challenge rules on nutrient use efficiency in trophic chains, account for herbivore outbreaks, or stabilize competitive interactions in lower trophic levels, and they may use cues derived from complex interaction networks to locate their hosts. This review focuses on the fascinating ecology of hyperparasitoids related to how they exploit and locate their often inconspicuous hosts and the insect community processes in which hyperparasitoids are prominent players. Expected final online publication date for the Annual Review of Entomology, Volume 67 is January 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Foraging animals face the difficult task to find resources in complex environments that contain conflicting information. The presence of a non-suitable resource that provides attractive cues can be expected to confuse foraging animals and to reduce their foraging efficiency. We used the parasitoid Cotesia glomerata to study the effect of non-host-infested plants and associative learning on parasitoid foraging efficiency. Inexperienced C. glomerata did not prefer volatiles emitted from host (Pieris brassicae)-infested plants over volatiles from non-host (Mamestra brassicae)-infested plants and parasitoids that had to pass non-host-infested plants needed eight times longer to reach the host-infested plant compared to parasitoids that had to pass undamaged plants. Contrary to our expectations, oviposition experience on a host-infested leaf decreased foraging efficiency due to more frequent visits of non-host-infested plants. Oviposition experience did not only increase the responsiveness of C. glomerata to the host-infested plants, but also the attraction towards herbivore-induced plant volatiles in general. Experience with non-host-infested leaves on the contrary resulted in a reduced attraction towards non-host-infested plants, but did not increase foraging efficiency. Our study shows that HIPVs emitted by non-host-infested plants can confuse foraging parasitoids and reduce their foraging efficiency when non-host-infested plants are abundant. Our results further suggest that the effect of experience on foraging efficiency in the presence of non-host-infested plants depends on the similarity between the rewarding and the non-rewarding cue as well as on the completeness of information that parasitoids have acquired about the rewarding and non-rewarding cues.

Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing hyperparasitoids to find their preferred hosts in heterogeneous environments. Electronic supplementary material The online version of this article (10.1007/s00442-019-04352-w) contains supplementary material, which is available to authorized users.

Plants balance the allocation of resources between growth and defence to optimize fitness in a competitive environment. Perception of neighbour‐detection cues, such as a low ratio of red to far‐red (R:FR) radiation, activates a suite of shade‐avoidance responses that include stem elongation and upward leaf movement, whilst simultaneously downregulating defence. This downregulation is hypothesized to benefit the plant either by mediating the growth‐defence balance in favour of growth in high plant densities or, alternatively, by mediating defence of individual leaves such that those most photosynthetically productive are best protected. To test these hypotheses, we used a 3D functional–structural plant model of Brassica nigra that mechanistically simulates the interactions between plant architecture, herbivory, and the light environment. Our results show that plant‐level defence expression is a strong determinant of plant fitness and that leaf‐level defence mediation by R:FR can provide a fitness benefit in high densities. However, optimal plant‐level defence expression does not decrease monotonically with plant density, indicating that R:FR mediation of defence alone is not enough to optimize defence between densities. Therefore, assessing the ecological significance of R:FR‐mediated defence is paramount to better understand the evolution of this physiological linkage and its implications for crop breeding.

Plant phenotypic plasticity in response to antagonists can affect other community members such as mutualists, conferring potential ecological costs associated with inducible plant defence. For flowering plants, induction of defences to deal with herbivores can lead to disruption of plant–pollinator interactions. Current knowledge on the full extent of herbivore‐induced changes in flower traits is limited, and we know little about specificity of induction of flower traits and specificity of effect on flower visitors. We exposed flowering Brassica nigra plants to six insect herbivore species and recorded changes in flower traits (flower abundance, morphology, colour, volatile emission, nectar quantity, and pollen quantity and size) and the behaviour of two pollinating insects. Our results show that herbivory can affect multiple flower traits and pollinator behaviour. Most plastic floral traits were flower morphology, colour, the composition of the volatile blend, and nectar production. Herbivore‐induced changes in flower traits resulted in positive, negative, or neutral effects on pollinator behaviour. Effects on flower traits and pollinator behaviour were herbivore species‐specific. Flowers show extensive plasticity in response to antagonist herbivores, with contrasting effects on mutualist pollinators. Antagonists can potentially act as agents of selection on flower traits and plant reproduction via plant‐mediated interactions with mutualists., We show that plant interactions with pollinators may be easily disrupted or enhanced by herbivores due to extensive floral plasticity. Herbivore‐species‐specific changes in flower morphology, colour, volatile blend, and nectar and pollen production had contrasting effects on pollinator behaviour.

As a result of co-evolution between plants and herbivores, related plants often interact with similar herbivore communities. Variation in plant–herbivore interactions is determined by variation in underlying functional traits and by ecological and stochastic processes. Hence, typically, only a subset of possible interactions is realised on individual plants. We show that insect herbivore communities assembling on individual plants are structured by plant phylogeny among 12 species in two phylogenetic lineages of Brassicaceae. This community sorting to plant phylogeny was retained when splitting the community according to herbivore feeding guilds. Relative abundance of herbivores as well as the size of the community structured community dissimilarity among plant species. Importantly, the amount of intraspecific variation in realised plant–herbivore interactions is also phylogenetically structured. We argue that variability in realised interactions that are not directly structured by plant traits is ecologically relevant and must be considered in the evolution of plant defences.

Tropospheric ozone is a highly oxidative pollutant with the potential to alter plant metabolism. The direct effects of ozone on plant phenotype may alter interactions with other organisms, such as pollinators, and, consequently, affect plant reproductive success. In a set of greenhouse experiments, we tested whether exposure of plants to a high level of ozone affected their phenological development, their attractiveness to four different pollinators (mason bees, honeybees, hoverflies and bumblebees) and, ultimately, their reproductive success. Exposure of plants to ozone accelerated flowering, particularly on plants that were growing in autumn, when light and temperature cues, that commonly promote flowering, were weaker. Simultaneously, there was a tendency for ozone-exposed plants to disinvest in vegetative growth. Plant exposure to ozone did not substantially affect pollinator preference, but bumblebees had a tendency to visit more flowers on ozone-exposed plants, an effect that was driven by the fact that these plants tended to have more open flowers, meaning a stronger attraction signal. Honeybees spent more time per flower on ozone-exposed plants than on control plants. Acceleration of flower production and the behavioural responses of pollinators to ozone-exposed plants resulted in retained reproductive fitness of plants pollinated by bumblebees, honeybees and mason bees, despite the negative effects of ozone on plant growth. Plants that were pollinated by hoverflies had a reduction in reproductive fitness in response to ozone. In a natural setting, acceleration of flowering by ozone might foster desynchronization between plant and pollinator activities. This can have a strong impact on plants with short flowering periods and on plants that, unlike wild mustard, lack compensatory mechanisms to cope with the absence of pollinator activity in the beginning of flowering.

Background The microbiome of many insects consists of a diverse community of microorganisms that can play critical roles in the functioning and overall health of their hosts. Although the microbial communities of insects have been studied thoroughly over the past decade, little is still known about how biotic interactions affect the microbial community structure in and on the bodies of insects. In insects that are attacked by parasites or parasitoids, it can be expected that the microbiome of the host insect is affected by the presence of these parasitic organisms that develop in close association with their host. In this study, we used high-throughput amplicon sequencing targeting both bacteria and fungi to test the hypothesis that parasitism by the endoparasitoid Cotesia glomerata affected the microbiome of its host Pieris brassicae. Healthy and parasitized caterpillars were collected from both natural populations and a laboratory culture. Results Significant differences in bacterial community structure were found between field-collected caterpillars and laboratory-reared caterpillars, and between the external and the internal microbiome of the caterpillars. Parasitism significantly altered the internal microbiome of caterpillars, but not the external microbiome. The internal microbiome of all parasitized caterpillars and of the parasitoid larvae in the caterpillar hosts was dominated by a Wolbachia strain, which was completely absent in healthy caterpillars, suggesting that the strain was transferred to the caterpillars during oviposition by the parasitoids. Conclusion We conclude that biotic interactions such as parasitism have pronounced effects on the microbiome of an insect host and possibly affect interactions with higher-order insects.

Plants are members of complex communities of which arthropods are the most speciose members. The role of carnivores in shaping the outcome of multi-trophic interactions by top-down control of herbivores has been well studied. Particularly, the positive impacts of natural enemies of herbivores on plants through direct (consumptive) and indirect (non-consumptive) effects on their prey and hosts have received considerable interest, while multi-trophic interactions that result in negative effects on plants have received little attention. Negative impacts of carnivorous arthropods have been documented and arise when carnivores directly affect plants and/or their interactions with beneficial arthropods. In general, negative effects may be compensated by positive effects of other carnivorous arthropods, but their presence and significance is likely to be underestimated in tri-trophic interactions. Recent studies have revealed that the composition and dynamics of the plant and arthropod community have a significant effect on plant fitness. Therefore, we encourage an approach that accounts for a larger community of species and interactions associated with plants, including interaction types in which carnivores may negatively affect plants. This review highlights specific interaction types that ultimately lead to negative effects of carnivores on plants. This synthesis presents alternative hypotheses to those that predict that carnivores invariably benefit plants. Testing potential costs and benefits of carnivores to plants will advance our understanding of indirect plant defence. A free Plain Language Summary can be found within the Supporting Information of this article.

As a result of co-evolution between plants and herbivores, related plants often interact with similar communities of herbivores. On individual plants, typically only a subset of interactions is realized. The stochasticity of realized interactions leads to uncertainty of attack on individual plants and is likely to determine adaptiveness of plant defence strategies. Here, we show that across 12 plant species in two phylogenetic lineages of the Brassicaceae, variation in realized herbivore communities reveals a phylogenetic signal in the uncertainty of attack on individual plants. Individual plants of Brassicaceae Lineage II were attacked by a larger number of herbivore species from a larger species pool, resulting in a higher uncertainty of realized antagonistic interactions compared to plants in Lineage I. We argue that uncertainty of attack in terms of realized interactions on individual plants is ecologically relevant and must therefore be considered in the evolution of plant defences.

Summary Evolutionary arms‐races between plants and insect herbivores have long been proposed to generate key innovations such as plant toxins and detoxification mechanisms that can drive diversification of the interacting species. A novel front‐line of plant defence is the killing of herbivorous insect eggs.We test whether an egg‐killing plant trait has an evolutionary basis in such a plant–insect arms‐race. Within the crucifer family (Brassicaceae), some species express a hypersensitive response (HR)‐like necrosis underneath butterfly eggs (Pieridae) that leads to eggs desiccating or falling off the plant. We studied the phylogenetic distribution of this trait, its egg‐killing effect on and elicitation by butterflies, by screening 31 Brassicales species, and nine Pieridae species.We show a clade‐specific induction of strong, egg‐killing HR‐like necrosis mainly in species of the Brassiceae tribe including Brassica crops and close relatives. The necrosis is strongly elicited by pierid butterflies that are specialists of crucifers. Furthermore, HR‐like necrosis is linked to PR1 defence gene expression, accumulation of reactive oxygen species and cell death, eventually leading to egg‐killing.Our findings suggest that the plants’ egg‐killing trait is a new front on the evolutionary arms‐race between Brassicaceae and pierid butterflies beyond the well‐studied plant toxins that have evolved against their caterpillars.

Biological pest control depends on the ability of natural enemies to find herbivore-infested plants, which is often guided by herbivore-induced plant volatiles (HIPVs). While foraging behavior of natural enemies has been extensively studied under controlled conditions, little is known on how odor-guided foraging behavior is influenced by fluctuating weather conditions in the field. Here we investigated how HIPV-guided foraging of Cotesia glomerata parasitoids is influenced by prevailing weather conditions in the field. C. glomerata females were released in 5 m radius circles of cabbage plants infested with Pieris brassicae caterpillars, and host finding success and direction of foraging activity was assessed by recapturing parasitoids on the host-infested plants. Wind speed and direction, humidity, barometric pressure and temperature was recorded and related to parasitoid foraging activity. Parasitoid foraging behavior was studied in more detail by observing individually released parasitoids in 0.5 m circles with host-infested cabbages. Recapture rates and movement direction of parasitoids was influenced by an interaction between humidity, wind speed, temperature and change in barometric pressure. High humidity and low wind speed was generally positively associated with host finding success. Direct observations of parasitoid flight behavior confirmed the influence of humidity and wind speed. Successful host finding in upwind direction was only observed at wind speeds below 3 m/s. Our study highlights the complex ways in which weather variables moderate parasitoid foraging behavior under field conditions. Since unfavorable weather conditions result in a strong reduction in parasitoid foraging efficiency, weather conditions are an important factor in the effectiveness of parasitoids as biocontrol agents.

A plant's offspring may escape unfavourable local conditions through seed dispersal. Whether plants use this strategy to escape insect herbivores is not well understood. Here, we explore how different dandelion ( Taraxacum officinale agg.) populations, including diploid outcrossers and triploid apomicts, modify seed dispersal in response to root herbivore attack by their main root-feeding natural enemy, the larvae of the common cockchafer Melolontha melolontha. In a manipulative field experiment, root herbivore attack increased seed dispersal potential through a reduction in seed weight in populations that evolved under high root herbivore pressure, but not in populations that evolved under low pressure. This increase in dispersal potential was independent of plant cytotype, but associated with a reduction in germination rate, suggesting that adapted dandelions trade dispersal for establishment upon attack by root herbivores. Analysis of vegetative growth parameters suggested that the increased dispersal capacity was not the result of stress flowering. In summary, these results suggest that root herbivory selects for an induced increase in dispersal ability in response to herbivore attack. Induced seed dispersal may be a strategy that allows adapted plants to escape from herbivores.

Parasitoids depend on other insects for the development of their offspring. Their eggs are laid in or on a host insect that is consumed during juvenile development. Parasitoids harbor a diversity of microbial symbionts including viruses, bacteria, and fungi. In contrast to symbionts of herbivorous and hematophagous insects, parasitoid symbionts do not provide nutrients. Instead, they are involved in parasitoid reproduction, suppression of host immune responses, and manipulation of the behavior of herbivorous hosts. Moreover, recent research has shown that parasitoid symbionts such as polydnaviruses may also influence plant-mediated interactions among members of plant-associated communities at different trophic levels, such as herbivores, parasitoids, and hyperparasitoids. This implies that these symbionts have a much more extended phenotype than previously thought. This review focuses on the effects of parasitoid symbionts on direct and indirect species interactions and the consequences for community ecology.

Plants need to deal with antagonists, such as herbivores, while maintaining interactions with mutualists, such as pollinators that help plants to maximize their reproductive output. Although many plant species have inducible defences to save metabolic costs of defence in the absence of herbivores, plant responses induced by herbivore attack can have ecological costs. For example, herbivore-induced responses can affect flower traits and alter interactions with flower visitors. Such plant-mediated interactions between herbivores and flower visitors can affect plant reproductive output. Current knowledge on the generality and specificity of plant-mediated herbivore-flower-visitor interactions and its consequences for plant fitness is limited. In this study, we investigated whether a broad range of herbivores feeding on the annual plant Brassica nigra affect interactions with flower visitors, whether the direction of interactions is predicted by the feeding modes (chewing and sap-feeding) and sites (above- and belowground) of the herbivores, and whether it results in fitness consequences for the plant. Our results show that attack of B. nigra by a range of different herbivores influenced plant interactions with mutualist pollinators and an antagonist florivore, the pollen beetle Meligethes aeneus. Pollinator community composition was affected by herbivory, whereas overall pollinator attraction was maintained. Pollinator community composition of uninfested plants differed from that of chewing and root herbivore-infested plants. Main responders in the pollinator communities to changes induced by herbivory were syrphid flies, bumblebees, and solitary bees. Although the preference of pollen beetle adults was not affected by herbivory, beetle larvae performed best on plants infested with the nematode Heterodera schachtii. The changes in pollinator community composition and syrphid fly visitation can explain the observed increase in seed set of root herbivore-infested plants. Interactions of flowering B. nigra plants with mutualist and antagonist insects are well integrated and conflicting interactions do not reduce reproductive output. Our results suggest some degree of specificity in herbivore-flower-visitor interactions with consequences for plant fitness. Specificity of plant responses were determined at the species level as well as the herbivore functional group level, and differed depending on the flower visitor. Because plant reproduction was affected by indirect plant-mediated interactions, these can potentially result in selection on plant strategies to optimize growth, defence and reproduction. A plain language summary is available for this article.

1. Parasitoids are known to utilise learning of herbivore-induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non-suitable herbivores (non-hosts). Simultaneous infestation of plants by hosts and non-hosts has been found to result in induction of HIPVs that differ from host-infested plants. Each non-host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non-host herbivore also contain the host. 2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non-hosts in the laboratory and in semi-field experiments. 3. In two-choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant-host-non-host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non-host caterpillar Mamestra brassicae or the non-host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non-host caterpillars or aphids in a semi-field situation. 4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.

1. Plants are frequently under attack by multiple insect herbivores, which may interact indirectly through herbivore-induced changes in the plant's phenotype. The identity, order, and timing of herbivore arrivals may influence the outcome of interactions between two herbivores. How these aspects affect, in turn, subsequently arriving herbivores that feed on double herbivore-induced plants has not been widely investigated. 2. This study tested whether the order and timing of arrival of two inducing herbivores from different feeding guilds affected the preference and performance of a subsequently arriving third herbivore, caterpillars of Mamestra brassicae L. (Lepidoptera: Noctuidae). Aphids [Brevicoryne brassicae L. (Hemiptera: Aphididae)] and caterpillars [Plutella xylostella L. (Lepidoptera: Yponomeutidae)] were introduced onto wild Brassica oleracea L. (Brassicaceae) plants in different sequences and with different arrival times. The effects of these plant treatments on M. brassicae caterpillars were assessed in pairwise preference tests and no-choice performance tests. 3. The caterpillars of M. brassicae preferred to feed from undamaged plants rather than double herbivore-induced plants. Compared with undamaged plants, they preferred plant material on which aphids had arrived first followed by caterpillars, whereas they avoided plant material with the reverse order of herbivore arrival. Performance of the caterpillars increased with increasing arrival time between herbivore infestations in double herbivore-induced plants. Although M. brassicae grew faster on plants induced by aphids than on those induced by caterpillars alone, its performance was not affected by the order of previous herbivore arrival. 4. These results imply that the timing of colonisation by multiple herbivores determines the outcome of plant-mediated herbivore-herbivore interactions.

Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta‐analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals., The project was supported by the Graduate School ‘Evolutionary Networks: Organisms, Reactions, Molecules’ (E‐Norm) of the Heinrich‐Heine‐University, Düsseldorf, Germany, the Max Planck Society and the Deutsche Forschungsgemeinschaft (DFG JU 2856/1‐1 and DFG JU 2856/2‐2).

Intraspecific plant diversity can modify the properties of associated arthropod communities and plant fitness. However, it is not well understood which plant traits determine these ecological effects. We explored the effect of intraspecific chemical diversity among neighbouring plants on the associated invertebrate community and plant traits. In a common garden experiment, intraspecific diversity among neighbouring plants was manipulated using three plant populations of wild cabbage that differ in foliar glucosinolates. Plants were larger, harboured more herbivores, but were less damaged when plant diversity was increased. Glucosinolate concentration differentially correlated with generalist and specialist herbivore abundance. Glucosinolate composition correlated with plant damage, while in polycultures, variation in glucosinolate concentrations among neighbouring plants correlated positively with herbivore diversity and negatively with plant damage levels. The results suggest that intraspecific variation in secondary chemistry among neighbouring plants is important in determining the structure of the associated insect community and positively affects plant performance.

Summary Herbivore‐induced plant volatiles (HIPVs) are an important cue used in herbivore location by carnivorous arthropods such as parasitoids. The effects of plant volatiles on parasitoids have been well characterised at small spatial scales, but little research has been done on their effects at larger spatial scales. The spatial matrix of volatiles (‘volatile mosaic’) within which parasitoids locate their hosts is dynamic and heterogeneous. It is shaped by the spatial pattern of HIPV‐emitting plants, the concentration, chemical composition and breakdown of the emitted HIPV blends, and by environmental factors such as wind, turbulence and vegetation that affect transport and mixing of odour plumes. The volatile mosaic may be exploited differentially by different parasitoid species, in relation to species traits such as sensory ability to perceive volatiles and the physical ability to move towards the source. Understanding how HIPVs influence parasitoids at larger spatial scales is crucial for our understanding of tritrophic interactions and sustainable pest management in agriculture. However, there is a large gap in our knowledge on how volatiles influence the process of host location by parasitoids at the landscape scale. Future studies should bridge the gap between the chemical and behavioural ecology of tritrophic interactions and landscape ecology.

A vast body of research demonstrates that many ecological and evolutionary processes can only be understood from a tri‐trophic viewpoint, that is, one that moves beyond the pairwise interactions of neighbouring trophic levels to consider the emergent features of interactions among multiple trophic levels. Despite its unifying potential, tri‐trophic research has been fragmented, following two distinct paths. One has focused on the population biology and evolutionary ecology of simple food chains of interacting species. The other has focused on bottom‐up and top‐down controls over the distribution of biomass across trophic levels and other ecosystem‐level variables. Here, we propose pathways to bridge these two long‐standing perspectives. We argue that an expanded theory of tri‐trophic interactions (TTIs) can unify our understanding of biological processes across scales and levels of organisation, ranging from species evolution and pairwise interactions to community structure and ecosystem function. To do so requires addressing how community structure and ecosystem function arise as emergent properties of component TTIs, and, in turn, how species traits and TTIs are shaped by the ecosystem processes and the abiotic environment in which they are embedded. We conclude that novel insights will come from applying tri‐trophic theory systematically across all levels of biological organisation., Tri‐trophic research has followed two distinct paths: One has focused on the population biology and evolutionary ecology of simple food chains of interacting species; the other has focused on bottom‐up and top‐down controls over the distribution of biomass across trophic levels and ecosystem‐level variables. Here, we provide a roadmap to bridge these two long‐standing perspectives and identify two key challenges. First, determining whether and how ecosystem‐level TTIs emerge from food chain‐ and community‐level TTIs. Second, determining whether and how ecosystem‐level processes and abiotic factors feedback to shape the species traits that drive TTIs.

Plants allow their offspring to escape unfavourable local conditions through seed dispersal. Whether plants use this strategy to escape herbivores is not well understood. Here, we explore how different Taraxacum officinale populations modify seed dispersal in response to root herbivore attack by Melolontha melolontha in the field. Root herbivore attack increases seed dispersal potential through a reduction in seed weight in populations that have evolved under high root herbivore pressure, but not in populations that have evolved under low pressure. This increase in dispersal potential is associated with reduced germination, suggesting that adapted plants trade dispersal for establishment. Analysis of vegetative growth parameters suggests that increased dispersal is not the result of stress flowering. These results suggest that root herbivory selects for genotypes that increase their dispersal ability in response to herbivore attack.

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore-induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host-location behaviour of parasitoids in detail in a semi-field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set-ups with 10 or 20 m intervals between plants. In the semi-field set-up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host-infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore-infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant-trait variation in HIPVs when studying animal foraging behaviour and multi-trophic interactions in a spatial context.

In perennial plants, interactions with other community members during the vegetative growth phase may influence community assembly during subsequent reproductive years and may influence plant fitness. It is well‐known that plant responses to herbivory affect community assembly within a growing season, but whether plant–herbivore interactions result in legacy effects on community assembly across seasons has received little attention. Moreover, whether plant–herbivore interactions during the vegetative growing season are important in predicting plant fitness directly or indirectly through legacy effects is poorly understood.Here, we tested whether plant–arthropod interactions in the vegetative growing season of perennial wild cabbage plants, Brassica oleracea, result in legacy effects in arthropod community assembly in the subsequent reproductive season and whether legacy effects have plant fitness consequences. We monitored the arthropod community on plants that had been induced with either aphids, caterpillars or no herbivores in a full‐factorial design across 2 years. We quantified the plant traits ‘height’, ‘number of leaves’ and ‘number of flowers’ to understand mechanisms that may mediate legacy effects. We measured seed production in the second year to evaluate plant fitness consequences of legacy effects.Although we did not find community responses to the herbivory treatments, our data show that community composition in the first year leaves a legacy on community composition in a second year: predator community composition co‐varied across years. Structural equation modelling analyses indicated that herbivore communities in the vegetative year correlated with plant performance traits that may have caused a legacy effect on especially predator community assembly in the subsequent reproductive year. Interestingly, the legacy of the herbivore community in the vegetative year predicted plant fitness better than the herbivore community that directly interacted with plants in the reproductive year. Synthesis. Thus, legacy effects of plant–herbivore interactions affect community assembly on perennial plants across growth seasons and these processes may affect plant reproductive success. We argue that plant–herbivore interactions in the vegetative phase as well as in the cross‐seasonal legacy effects caused by plant responses to arthropod herbivory may be important in perennial plant trait evolution such as ontogenetic variation in growth and defence strategies.

Plant phenotypic plasticity in response to herbivore attack includes changes in flower traits. Such herbivore-induced changes in flower traits have consequences for interactions with flower visitors. We synthesize here current knowledge on the specificity of herbivore-induced changes in flower traits, the underlying molecular mechanisms, and the ecological consequences for flower-associated communities. Herbivore-induced changes in flower traits seem to be largely herbivore species-specific. The extensive plasticity observed in flowers influences a highly connected web of interactions within the flower-associated community. We argue that the adaptive value of herbivore-induced plant responses and flower plasticity can be fully understood only from a community perspective rather than from pairwise interactions.

Herbivore attack can alter plant interactions with pollinators, ranging from reduced to enhanced pollinator visitation. The direction and strength of effects of herbivory on pollinator visitation could be contingent on the type of plant tissue or organ attacked by herbivores, but this has seldom been tested experimentally. We investigated the effect of variation in feeding site of herbivorous insects on the visitation by insect pollinators on flowering Brassica nigra plants. We placed herbivores on either leaves or flowers, and recorded the responses of two pollinator species when visiting flowers. Our results show that variation in herbivore feeding site has profound impact on the outcome of herbivore–pollinator interactions. Herbivores feeding on flowers had consistent positive effects on pollinator visitation, whereas herbivores feeding on leaves did not. Herbivores themselves preferred to feed on flowers, and mostly performed best on flowers. We conclude that herbivore feeding site choice can profoundly affect herbivore–pollinator interactions and feeding site thereby makes for an important herbivore trait that can determine the linkage between antagonistic and mutualistic networks. Electronic supplementary material The online version of this article (10.1007/s00442-019-04539-1) contains supplementary material, which is available to authorized users.