Aboveground Insect Herbivores Research Articles

Diverse cropping systems lead to higher larval mortality of the cabbage root fly (Delia radicum)

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.

Insect exuviae as soil amendment affect flower reflectance and increase flower production and plant volatile emission.

Soil composition and herbivory are two environmental factors that can affect plant traits including flower traits, thus potentially affecting plant-pollinator interactions. Importantly, soil composition and herbivory may interact in these effects, with consequences for plant fitness. We assessed the main effects of aboveground insect herbivory and soil amendment with exuviae of three different insect species on visual and olfactory traits of Brassica nigra plants, including interactive effects. We combined various methodological approaches including gas chromatography/mass spectrometry, spectroscopy and machine learning to evaluate changes in flower morphology, colour and the emission of volatile organic compounds (VOCs). Soil amended with insect exuviae increased the total number of flowers per plant and VOC emission, whereas herbivory reduced petal area and VOC emission. Soil amendment and herbivory interacted in their effect on the floral reflectance spectrum of the base part of petals and the emission of 10 VOCs. These findings demonstrate the effects of insect exuviae as soil amendment on plant traits involved in reproduction, with a potential for enhanced reproductive success by increasing the strength of signals attracting pollinators and by mitigating the negative effects of herbivory.

Aboveground herbivory does not affect mycorrhiza-dependent nitrogen acquisition from soil but inhibits mycorrhizal network-mediated nitrogen interplant transfer in maize.

Arbuscular mycorrhizal fungi (AMF) are considered biofertilizers for sustainable agriculture due to their ability to facilitate plant uptake of important mineral elements, such as nitrogen (N). However, plant mycorrhiza-dependent N uptake and interplant transfer may be highly context-dependent, and whether it is affected by aboveground herbivory remains largely unknown. Here, we used 15N labeling and tracking to examine the effect of aboveground insect herbivory by Spodoptera frugiperda on mycorrhiza-dependent N uptake in maize (Zea mays L.). To minimize consumption differences and 15N loss due to insect chewing, insect herbivory was simulated by mechanical wounding and oral secretion of S. frugiperda larvae. Inoculation with Rhizophagus irregularis (Rir) significantly improved maize growth, and N/P uptake. The 15N labeling experiment showed that maize plants absorbed N from soils via the extraradical mycelium of mycorrhizal fungi and from neighboring plants transferred by common mycorrhizal networks (CMNs). Simulated aboveground leaf herbivory did not affect mycorrhiza-mediated N acquisition from soil. However, CMN-mediated N transfer from neighboring plants was blocked by leaf simulated herbivory. Our findings suggest that aboveground herbivory inhibits CMN-mediated N transfer between plants but does not affect N acquisition from soil solutions via extraradical mycorrhizal mycelium.

A Meta-analysis of Interactions Between Insect Herbivores and Plant-Parasitic Nematodes.

Insect herbivores and plant-parasitic nematodes are global, economically devastating pests that are present in nearly every crop and natural system worldwide. Although they may be spatially separated, they indirectly interact with each other by altering both plant chemical defense and nutrition. However, the outcome of these interactions is highly variable across different focal species. We performed a meta-analysis to determine how plant and nematode traits influence insect herbivore growth and reproduction, as well as nematode abundance and reproduction. We investigated how interactions between plant-parasitic nematodes and insect herbivores influence plant biomass, carbon, and nitrogen in the roots and shoots. We found no overall effect of nematodes on insect herbivores or insect herbivores on nematodes. However, while phloem-feeding insect reproduction was not affected by nematode feeding guild or plant family, chewing insect growth increased in the presence of cyst nematodes and decreased in the presence of gall nematodes. The effect of nematodes on chewing insect herbivore growth was also affected by the focal plant family. Nematode presence did not alter plant biomass when plants were exposed to aboveground insect herbivory, but carbon and nitrogen were higher in roots and nitrogen was higher in shoots of plants with nematodes and insects compared to plants with insects alone. Our results indicate that the mechanisms driving the outcome of aboveground-belowground interactions are still unclear, but those chewing insects may have more variable responses to nematode damage than phloem-feeders.

Effects of soil biota on growth, resistance and tolerance to herbivory in Triadica sebifera plants

Interactions with soil microbes can strongly affect plant growth and defense against aboveground herbivores. Plant species often accumulate specific soil pathogens in their rhizosphere, leading to reduced growth of plants in soils originating from stands of conspecific plants compared to soils from heterospecific plants. However, whereas effects of such conspecific vs. heterospecific soil biota on plant growth have been well documented, their effects on plant resistance and tolerance to aboveground insect herbivores have not. We compared growth and defense of Triadica sebifera plants from populations where the species is native (China), when grown in sterilized soils, or in soils harbouring belowground biota from conspecific (native Triadica) or heterospecific (native grass) soils. In each of these soils, plants were exposed to a 15-day period of foliar herbivory by a specialist weevil (Heterapoderopsis bicallosicollis), a specialist caterpillar (Gadirtha inexacta), or no herbivory (cage), followed by a 60-day recovery period. Soil biota from conspecific and hetetospecific soils differed in their effects on plant growth and defense. First, in the absence of herbivory, soil biota from heterospecific soils slightly enhanced plant growth, whereas those from conspecific soils strongly reduced plant growth. Second, soil biota from conspecific soils strongly affected plant resistance and tolerance to foliar herbivory, whereas soil biota from heterospecific plants did not. The effects of soil biota on plant defense were herbivore-specific. In particular, conspecific soil biota reduced resistance to caterpillar but not to weevil feeding, whereas they enhanced tolerance to weevil but not to caterpillar feeding. Conspecific soil biota also mitigated induction of root flavonoids by herbivores and led to reduced root phenolics in response to herbivory. Conversely, caterpillar feeding increased AMF colonization, but under these conditions, AMF colonization was negatively associated with plant biomass. In addition to testing effects on native plants, we also tested effects of native soil biota on growth and resistance of plants from the introduced range (North America). Plants from the introduced range had higher shoot production, shoot-to-root ratio, and leaf phenolic and flavonoid production than plants from the native range, but their interactions with soil biota showed only minor differences compared to plants from the native range. Our results suggest that incorporating the effects of soil biota in interactions between plants and foliar herbivores is critical for understanding variations in growth, defense, and performance among plant populations at local and broader geographic scales.

Aboveground herbivory increases soil nematode abundance of an invasive plant

Abstract Aims Plant invasions have the potential to affect the community structure of soil nematodes, but little is known about whether such effects are mediated by aboveground herbivores since invasive plants are not completely released from herbivores in the introduced range. In this study, we explored how aboveground insect herbivores mediated the effect of invasive plant Alternanthera philoxeroides on soil nematodes and examined the temporal variations of such an herbivory-elicited effect. Methods We conducted a greenhouse experiment by applying different herbivory treatments (no insect herbivores, specialist Agasicles hygrophila and generalist Cassida piperata) to potted A. philoxeroides, and then measured the community compositions of soil nematodes in corresponding pots on the 1st, 10th and 20th day after removal of all herbivores. In addition, the carbon content of roots and root exudate of A. philoxeroides were also measured. Important Findings Our results showed that aboveground herbivory significantly increased the abundance of soil nematodes of A. philoxeroides, likely plant feeder nematodes, after insect herbivores were removed immediately (1st day). However, such impacts waned with time and there was no significant difference at later stages (10th and 20th days). Furthermore, the effects of specialist A. hygrophila and generalist C. piperata herbivory were consistent on the abundance of soil nematodes. Overall, our results suggest that aboveground insect herbivores have the potential to alter the effects of plant invasions on soil nematodes, but such impacts are transient. Furthermore, our study highlighted the importance of integrating the effects of above- and belowground organisms when evaluating the impacts of plant invasions.

Altered rainfall patterns reduce plant fitness and disrupt interactions between below‐ and aboveground insect herbivores

AbstractEvidence is accumulating of the disruptive effects of climate change on species interactions. However, little is known about how changes in climate patterns, such as temporal shifts in rainfall events, will affect multitrophic interactions. Here, we investigated the effects of changes in rainfall patterns on the interactions between root herbivores, a plant, and its associated aboveground insects in a semiarid region by experimentally manipulating in the field rainfall intensity and frequency. We found that a shift in rainfall severely constrained biomass acquisition and flowering of the plant Moricandia moricandioides, resulting in fitness reduction. Importantly, enhanced rainfall affected the interactions between below‐ and some aboveground herbivores, disrupting the positive effects of root herbivores on chewing insects. The shifts in precipitation had also plant‐mediated consequences for planthoppers, the dominant sapsuckers in our study system. A combination of mechanisms involving biomass acquisition and plant defenses seemed to be responsible for the different responses of insects and their interactions with the plant. This study provides evidence that altered rainfall patterns due to climate change affect not only trophic groups differentially but also their interactions.

Plant-soil feedback effects altered by aboveground herbivory explain plant species abundance in the landscape.

Relatively little is known about how plant-soil feedbacks (PSFs) may affect plant growth in field conditions where factors such as herbivory may be important. Using a potted experiment in a grassland, we measured PSFs with and without aboveground insect herbivory for 20 plant species. We then compared PSF values to plant landscape abundance. Aboveground herbivory had a large negative effect on PSF values. For 15 of 20 species, PSFs were more negative with herbivory than without. This occurred because plant biomass on "home" soils was smaller with herbivory than without. PSF values with herbivory were correlated with plant landscape abundance, whereas PSF values without herbivory were not. Shoot nitrogen concentrations suggested that plants create soils that increase nitrogen uptake, but that greater shoot nitrogen values increase herbivory and that the net effect of positive PSF and greater aboveground herbivory is less aboveground biomass. Results provided clear evidence that PSFs alone have limited power in explaining species abundances and that herbivory has stronger effects on plant biomass and growth on the landscape. Our results provide a potential explanation for observed differences between greenhouse and field PSF experiments and suggest that PSF experiments need to consider important biotic interactions, like aboveground herbivory, particularly when the goal of PSF research is to understand plant growth in field conditions.

Plant traits shape soil legacy effects on individual plant–insect interactions

Plant‐mediated soil legacy effects can be important determinants of the performance of plants and their aboveground insect herbivores, but, soil legacy effects on plant–insect interactions have been tested for only a limited number of host plant species and soils. Here, we tested the performance of a polyphagous aboveground herbivore, caterpillars of the cabbage moth Mamestra brassicae, on twelve host plant species that were grown on a set of soils conditioned by each of these twelve species. We tested how growth rate (fast‐ or slow‐growing) and functional type (grass or forb) of the plant species that conditioned the soil and of the responding host plant species growing in those soils affect the response of insect herbivores to conditioned soils. Our results show that plants and insect herbivores had lower biomass in soils that were conditioned by fast‐growing forbs than in soils conditioned by slow‐growing forbs. In soils conditioned by grasses, growth rate of the conditioning plant had the opposite effect, i.e. plants and herbivores had higher biomass in soils conditioned by fast‐growing grasses, than in soils conditioned by slow‐growing grasses. We show that the response of aboveground insects to soil legacy effects is strongly positively correlated with the response of the host plant species, indicating that plant vigour may explain these relationships. We provide evidence that soil communities can play an important role in shaping plant–insect interactions aboveground. Our results further emphasize the important and interactive role of the conditioning and the response plant in mediating soil–plant–insect interactions.

A growth-defense trade-off is general across native and exotic grasses.

High-resource environments typically favor quick-growing, poorly defended plants, while resource-poor environments typically favor slow-growing, well-defended plants. The prevailing hypothesis explaining this pattern states that, as resource availability increases, well-defended, slow-growing species are replaced by poorly defended, fast-growing species. A second hypothesis states that greater resource availability increases allocation to growth at the expense of defense, within species. Regardless of mechanism, if exotic species are released from enemies relative to natives, shifts in allocation to growth and defense both within and among species could differ by geographic provenance. To test whether resource availability alters growth or defense, within and among species, and whether any such effects differ between natives and exotics, we manipulated soil nutrient supply and access of aboveground insect herbivores and fungal pathogens under field conditions to individuals of six native and six exotic grass species that co-occurred in a North Carolina old field. The prevailing hypothesis' prediction-that species-level enemy impact increases with species' nutrient responsiveness-was confirmed. Moreover, this relationship did not differ between native and exotic species. The second hypothesis' prediction-that individual-level enemy impact increases with nutrient supply, after accounting for species-level variation in performance-was not supported. Together, these results support the idea, across native and exotic species, that plant species turnover is the primary mechanism underlying effects of nutrient enrichment on allocation to growth and defense in plant communities.

Aphids Influence Soil Fungal Communities in Conventional Agricultural Systems.

Arbuscular mycorrhizal fungi (AMF) form symbioses with the roots of most plant species, including cereals. AMF can increase the uptake of nutrients including nitrogen (N) and phosphorus (P), and of silicon (Si) as well as increase host resistance to various stresses. Plants can simultaneously interact with above-ground insect herbivores such as aphids, which can alter the proportion of plant roots colonized by AMF. However, it is unknown if aphids impact the structure of AMF communities colonizing plants or the extent of the extraradical mycelium produced in the soil, both of which can influence the defensive and nutritional benefit a plant derives from the symbiosis. This study investigated the effect of aphids on the plant-AMF interaction in a conventionally managed agricultural system. As plants also interact with other soil fungi, the non-AMF fungal community was also investigated. We hypothesized that aphids would depress plant growth, and reduce intraradical AMF colonization, soil fungal hyphal density and the diversity of AM and non-AM fungal communities. To test the effects of aphids, field plots of barley enclosed with insect proof cages were inoculated with Sitobion avenae or remained uninoculated. AMF specific and total fungal amplicon sequencing assessed root fungal communities 46 days after aphid addition. Aphids did not impact above-ground plant biomass, but did increase the grain N:P ratio. Whilst aphid presence had no impact on AMF intraradical colonization, soil fungal hyphal length density, or AMF community characteristics, there was a trend for the aphid treatment to increase vesicle numbers and the relative abundance of the AMF family Gigasporaceae. Contrary to expectations, the aphid treatment also increased the evenness of the total fungal community. This suggests that aphids can influence soil communities in conventional arable systems, a result that could have implications for multitrophic feedback loops between crop pests and soil organisms across the above-below-ground interface.

The relative importance of plant-soil feedbacks for plant-species performance increases with decreasing intensity of herbivory.

Under natural conditions, aboveground herbivory and plant-soil feedbacks (PSFs) are omnipresent interactions strongly affecting individual plant performance. While recent research revealed that aboveground insect herbivory generally impacts the outcome of PSFs, no study tested to what extent the intensity of herbivory affects the outcome. This, however, is essential to estimate the contribution of PSFs to plant performance under natural conditions in the field. Here, we tested PSF effects both with and without exposure to aboveground herbivory for four common grass species in nine grasslands that formed a gradient of aboveground invertebrate herbivory. Without aboveground herbivores, PSFs for each of the four grass species were similar in each of the nine grasslands-both in direction and in magnitude. In the presence of herbivores, however, the PSFs differed from those measured under herbivory exclusion, and depended on the intensity of herbivory. At low levels of herbivory, PSFs were similar in the presence and absence of herbivores, but differed at high herbivory levels. While PSFs without herbivores remained similar along the gradient of herbivory intensity, increasing herbivory intensity mostly resulted in neutral PSFs in the presence of herbivores. This suggests that the relative importance of PSFs for plant-species performance in grassland communities decreases with increasing intensity of herbivory. Hence, PSFs might be more important for plant performance in ecosystems with low herbivore pressure than in ecosystems with large impacts of insect herbivores.

Mechanisms and ecological implications of plant-mediated interactions between belowground and aboveground insect herbivores

Plant-mediated interactions between belowground (BG) and aboveground (AG) herbivores have received increasing interest recently. However, the molecular mechanisms underlying ecological consequences of BG–AG interactions are not fully clear yet. Herbivore-induced plant defenses are complex and comprise phytohormonal signaling, gene expression and production of defensive compounds (defined here as response levels), each with their own temporal dynamics. Jointly they shape the response that will be expressed. However, because different induction methods are used in different plant-herbivore systems, and only one or two response levels are measured in each study, our ability to construct a general framework for BG–AG interactions remains limited. Here we aim to link the mechanisms to the ecological consequences of plant-mediated interactions between BG and AG insect herbivores. We first outline the molecular mechanisms of herbivore-induced responses involved in BG–AG interactions. Then we synthesize the literature on BG–AG interactions in two well-studied plant-herbivore systems, Brassica spp. and Zea mays, to identify general patterns and specific differences. Based on this comprehensive review, we conclude that phytohormones can only partially mimic induction by real herbivores. BG herbivory induces resistance to AG herbivores in both systems, but only in maize this involves drought stress responses. This may be due to morphological and physiological differences between monocotyledonous (maize) and dicotyledonous (Brassica) species, and differences in the feeding strategies of the herbivores used. Therefore, we strongly recommend that future studies explicitly account for these basic differences in plant morphology and include additional herbivores while investigating all response levels involved in BG–AG interactions.

Aboveground insect herbivory increases plant competitive asymmetry, while belowground herbivory mitigates the effect.

Insect herbivores can shift the composition of a plant community, but the mechanism underlying such shifts remains largely unexplored. A possibility is that insects alter the competitive symmetry between plant species. The effect of herbivory on competition likely depends on whether the plants are subjected to aboveground or belowground herbivory or both, and also depends on soil nitrogen levels. It is unclear how these biotic and abiotic factors interactively affect competition. In a greenhouse experiment, we measured competition between two coexisting grass species that respond differently to nitrogen deposition: Dactylis glomerata L., which is competitively favoured by nitrogen addition, and Festuca rubra L., which is competitively favoured on nitrogen-poor soils. We predicted: (1) that aboveground herbivory would reduce competitive asymmetry at high soil nitrogen by reducing the competitive advantage of D. glomerata; and (2), that belowground herbivory would relax competition at low soil nitrogen, by reducing the competitive advantage of F. rubra. Aboveground herbivory caused a 46% decrease in the competitive ability of F. rubra, and a 23% increase in that of D. glomerata, thus increasing competitive asymmetry, independently of soil nitrogen level. Belowground herbivory did not affect competitive symmetry, but the combined influence of above- and belowground herbivory was weaker than predicted from their individual effects. Belowground herbivory thus mitigated the increased competitive asymmetry caused by aboveground herbivory. D. glomerata remained competitively dominant after the cessation of aboveground herbivory, showing that the influence of herbivory continued beyond the feeding period. We showed that insect herbivory can strongly influence plant competitive interactions. In our experimental plant community, aboveground insect herbivory increased the risk of competitive exclusion of F. rubra. Belowground herbivory appeared to mitigate the influence of aboveground herbivory, and this mechanism may play a role for plant species coexistence.

Roots under attack: contrasting plant responses to below- and aboveground insect herbivory.

The distinctive ecology of root herbivores, the complexity and diversity of root-microbe interactions, and the physical nature of the soil matrix mean that plant responses to root herbivory extrapolate poorly from our understanding of responses to aboveground herbivores. For example, root attack induces different changes in phytohormones to those in damaged leaves, including a lower but more potent burst of jasmonates in several plant species. Root secondary metabolite responses also differ markedly, although patterns between roots and shoots are harder to discern. Root defences must therefore be investigated in their own ecophysiological and evolutionary context, specifically one which incorporates root microbial symbionts and antagonists, if we are to better understand the battle between plants and their hidden herbivores.

Variation in plant-mediated interactions between rhizobacteria and caterpillars: potential role of soil composition.

Selected strains of non-pathogenic rhizobacteria can trigger induced systemic resistance (ISR) in plants against aboveground insect herbivores. However, the underlying mechanisms of plant-mediated interactions between rhizobacteria and herbivorous insects are still poorly understood. Using Arabidopsis thaliana Col-0-Pseudomonas fluorescens WCS417r as a model system, we investigated the performance and the molecular mechanisms underlying plant-mediated effects of rhizobacteria on the generalist caterpillar Mamestra brassicae and the specialist Pieris brassicae. Rhizobacteria colonisation of Arabidopsis roots resulted in decreased larval weight of M.brassicae, whereas no effect was observed on larval weight of P.brassicae. Using a jasmonic acid (JA)-impaired mutant (dde2-2), we confirmed the importance of JA in rhizobacteria-mediated ISR against M.brassicae. Interestingly, in some experiments we also observed rhizobacteria-induced systemic susceptibility to M.brassicae. The role of soil composition in the variable outcomes of microbe-plant-insect interactions was then assessed by comparing M.brassicae performance and gene transcription in plants grown in potting soil or a mixture of potting soil and sand in a 1:1 ratio. In a mixture of potting soil and sand, rhizobacteria treatment had a consistent negative effect on M.brassicae, whereas the effect was more variable in potting soil. Interestingly, at 24h post-infestation (hpi) rhizobacteria treatment primed plants grown in a mixture of potting soil and sand for stronger expression of the JA- and ethylene-regulated genes PDF1.2 and HEL, respectively. Our study shows that soil composition can modulate rhizobacteria-plant-insect interactions, and is a factor that should be considered when studying these belowground-aboveground interactions.

Impact of nitrogen fixing and plant growth-promoting bacteria on a phloem-feeding soybean herbivore

In soybean (Glycine max L.) production systems, growers often inoculate seeds with the symbiotic N-fixing species Bradyrhizobium japonicum along with other bacterial species or chemicals intended to enhance plant growth and yield. However, microbes associated with plant roots can also impact the biology of above-ground insect herbivores through influencing various aspects of plant physiology, with effects dependent on the bacterial species. Because rhizobial seed inoculants can potentially affect densities of soybean herbivores, we investigated the performance of phloem-feeding soybean aphids (Aphis glycines Matsumura) on: (1) soybeans receiving one of four commercially available rhizobial seed inoculants, (2) non-inoculated soybeans associated with existing soil bacteria, or (3) non-inoculated soybeans receiving high levels of fertilizer to suppress N-fixation while still providing adequate N as nitrate. We quantified effects of inoculants and aphid presence on parameters associated with plant growth, N-fixation, and foliar N levels, and explored relationships between aphid densities and these plant parameters. Regardless of inoculation treatment, aphid presence negatively affected plant biomass, pod density, and total N concentration in aerial plant tissues, although, effects on the concentration of ureide N (primary products of N-fixation) were not significant. Inoculant identity significantly impacted aphid populations in both short- (1 week) and longer-term experiments (2 months), with pest densities negatively related to the number of root nodules per plant. This research indicates that nodulation status of soybeans can influence above-ground herbivores.

Emerging role of roots in plant responses to aboveground insect herbivory

Plants have evolved complex biochemical mechanisms to counter threats from insect herbivory. Recent research has revealed an important role of roots in plant responses to above ground herbivory (AGH). The involvement of roots is integral to plant resistance and tolerance mechanisms. Roots not only play an active role in plant defenses by acting as sites for biosynthesis of various toxins and but also contribute to tolerance by storing photoassimilates to enable future regrowth. The interaction of roots with beneficial soil-borne microorganisms also influences the outcome of the interaction between plant and insect herbivores. Shoot-to-root communication signals are critical for plant response to AGH. A better understanding of the role of roots in plant response to AGH is essential in order to develop a comprehensive picture of plant-insect interactions. Here, we summarize the current status of research on the role of roots in plant response to AGH and also discuss possible signals involved in shoot-to-root communication.

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.

Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms.

In terrestrial food webs, the study of multitrophic interactions traditionally has focused on organisms that share a common domain, mainly above ground. In the last two decades, it has become clear that to further understand multitrophic interactions, the barrier between the belowground and aboveground domains has to be crossed. Belowground organisms that are intimately associated with the roots of terrestrial plants can influence the levels of primary and secondary chemistry and biomass of aboveground plant parts. These changes, in turn, influence the growth, development, and survival of aboveground insect herbivores. The discovery that soil organisms, which are usually out of sight and out of mind, can affect plant-herbivore interactions aboveground raised the question if and how higher trophic level organisms, such as carnivores, could be influenced. At present, the study of above-belowground interactions is evolving from interactions between organisms directly associated with the plant roots and shoots (e.g., root feeders - plant - foliar herbivores) to interactions involving members of higher trophic levels (e.g., parasitoids), as well as non-herbivorous organisms (e.g., decomposers, symbiotic plant mutualists, and pollinators). This multitrophic approach linking above- and belowground food webs aims at addressing interactions between plants, herbivores, and carnivores in a more realistic community setting. The ultimate goal is to understand the ecology and evolution of species in communities and, ultimately how community interactions contribute to the functioning of terrestrial ecosystems. Here, we summarize studies on the effects of root feeders on aboveground insect herbivores and parasitoids and discuss if there are common trends. We discuss the mechanisms that have been reported to mediate these effects, from changes in concentrations of plant nutritional quality and secondary chemistry to defense signaling. Finally, we discuss how the traditional framework of fixed paired combinations of root- and shoot-related organisms feeding on a common plant can be transformed into a more dynamic and realistic framework that incorporates community variation in species, densities, space and time, in order to gain further insight in this exciting and rapidly developing field.