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Provision of additional floral resources in the crop is a successful strategy of conservation biological control for attracting several natural enemies including predatory syrphids. However, the selection of flower species is mainly based on visiting preferences, paying little attention to the link between preference and performance. In this study, we assess the influence of feeding on flowers of two insectary plants (sweet alyssum and coriander) and flowers of a crop species (sweet pepper) on performance of the parental and first generation of the syrphid Sphaerophoria rueppellii (Wiedemann) (Diptera: Syrphidae). We found that floral preference of the adults was linked to developmental performance of their offspring. Sweet alyssum was the flower most frequently visited by syrphid adults, enhancing adult body size and egg-to adult survival of the F1 generation. RAJ gratefully acknowledges funding through the JAE Predoc CSIC scholarship program (JAEPre_08_00457). The Authors acknowledge the financial support from the Spanish Ministry of Science and Education (AGL2005-01449/AGR project).

As sexual selection is a coevolutionary process between males and females, various morphological and behavioral traits have evolved in each sex. In the tetranychid mites Tetranychus urticae Koch and T. kanzawai Kishida (Acari: Tetranychidae), males can mate repeatedly, whereas females normally accept only the first copulation for fertilization. Since early times, it had been reported that males engage in precopulatory mate guarding and combat against conspecifics for females to enhance their reproductive success. On the other hand, it was believed that females do not have opportunities to choose their mates. In the last 10 or so years, however, several new findings related to mating behavior were reported. Some of the findings reinforce our established knowledge, whereas some of them explode it. Here, I review the mating behavior of T. urticae and T. kanzawai by incorporating recent findings and then propose a new direction for future research.

Herbivore-induced plant volatiles are often involved in direct and indirect plant defence against herbivores. Linalool is a common floral scent and found to be released from leaves by many plants after herbivore attack. In this study, a linalool/nerolidol synthase, FaNES1, was overexpressed in the plastids of chrysanthemum plants (Chrysanthemum morifolium). The volatiles of FaNES1 chrysanthemum leaves were strongly dominated by linalool, but they also emitted small amount of the C11-homoterpene, (3E)-4,8-dimethyl-1,3,7-nonatriene, a derivative of nerolidol. Four nonvolatile linalool glycosides in methanolic extracts were found to be significantly increased in the leaves of FaNES1 plants compared to wild-type plants. They were putatively identified by LC-MS-MS as two linalool-malonyl-hexoses, a linalool-pentose-hexose and a glycoside of hydroxy-linalool. A leaf-disc dual-choice assay with western flower thrips (WFT, Frankliniella occidentalis) showed, initially during the first 15 min of WFT release, that FaNES1 plants were significantly preferred. This gradually reversed into significant preference for the control, however, at 20-28 h after WFT release. The initial preference was shown to be based on the linalool odour of FaNES1 plants by olfactory dual-choice assays using paper discs emitting pure linalool at similar rates as leaf discs. The reversal of preference into deterrence could be explained by the initial nonvolatile composition of the FaNES1 plants, as methanolic extracts were less preferred by WFT. Considering the common occurrence of linalool and its glycosides in plant tissues, it suggests that plants may balance attractive fragrance with 'poor taste' using the same precursor compound.

BACKGROUND: Most insect-resistant transgenic crops employ toxins to control pests. A novel approach is to enhance the effectiveness of natural enemies by genetic engineering of the biosynthesis of volatile organic compounds (VOCs). Before the commercialisation of such transgenic plants can be pursued, detailed fundamental studies of their effects on herbivores and their natural enemies are necessary. The linalool/nerolidol synthase gene FaNES1 was constitutively expressed from strawberry in three Arabidopsis thaliana accessions, and the behaviour of the aphid Brevicoryne brassicae L., the parasitoid Diaeretiella rapae McIntosh and the predator Episyrphus balteatus de Geer was studied. RESULTS: Transgenic FaNES1-expressing plants emitted (E)-nerolidol and larger amounts of (E)-DMNT and linalool. Brevicoryne brassicae was repelled by the transgenic lines of two of the accessions, whereas its performance was not affected. Diaeretiella rapae preferred aphid-infested transgenic plants over aphid-infested wild-type plants for two of the accessions. In contrast, female E. balteatus predators did not differentiate between aphid-infested transgenic or wild-type plants. CONCLUSION: The results indicate that the genetic engineering of plants to modify their emission of VOCs holds considerable promise for facilitating biological control of herbivores. Validation for crop plants is a necessary next step to assess the usefulness of modified volatile emission in integrated pest management.

The performance of natural enemies, such as parasitoid wasps, is affected by differences in the quality of the host’s diet, frequently mediated by species or population-related differences in plant allelochemistry. Here, we compared survival, development time, and body mass in a generalist herbivore, the cabbage moth, Mamestra brassicae, and its solitary endoparasitoid, Microplitis mediator, when reared on two cultivated (CYR and STH) and three wild (KIM, OH, and WIN) populations of cabbage, Brassica oleracea. Plants either were undamaged or induced by feeding of larvae of the cabbage butterfly, Pieris rapae. Development and biomass of M. brassicae and Mi. mediator were similar on both cultivated and one wild cabbage population (KIM), intermediate on the OH population, and significantly lower on the WIN population. Moreover, development was prolonged and biomass was reduced on herbivore-induced plants. However, only the survival of parasitized hosts (and not that of healthy larvae) was affected by induction. Analysis of glucosinolates in leaves of the cabbages revealed higher levels in the wild populations than cultivars, with the highest concentrations in WIN plants. Multivariate statistics revealed a negative correlation between insect performance and total levels of glucosinolates (GS) and levels of 3-butenyl GS. However, GS chemistry could not explain the reduced performance on induced plants since only indole GS concentrations increased in response to herbivory, which did not affect insect performance based on multivariate statistics. This result suggests that, in addition to aliphatic GS, other non- GS chemicals are responsible for the decline in insect performance, and that these chemicals affect the parasitoid more strongly than the host. Remarkably, when developing on WIN plants, the survival of Mi. mediator to adult eclosion was much higher than in its host, M. brassicae. This may be due to the fact that hosts parasitized by Mi. mediator pass through fewer instars, and host growth is arrested when they are only a fraction of the size of healthy caterpillars. Certain aspects of the biology and life-history of the host and parasitoid may determine their response to chemical challenges imposed by the food plant.

A central issue in the evolutionary ecology of species interactions is coevolution, which involves the reciprocal selection between individuals of interacting species. Understanding the importance of coevolution in shaping species interactions requires the consideration of spatial variation in their strength. This is exactly what the, recently developed, geographic mosaic theory of coevolution addresses. Another major development in the study of population ecology is the introduction of the population genomics approach in this field of research. This approach addresses spatial processes through molecular methods. It is of particular interest that population genomics is especially applicable to natural populations of non-model species. We describe how population genomics can be used in the context of the geographic mosaic of coevolution, specifically to identify coevolutionary hot-spots, and to attribute genetic variation found at specific loci to processes of selection versus trait remixing. The proposed integration of the population genomics approach with the conceptual framework of the geographic mosaic of coevolution is illustrated with a few selected, particularly demonstrative, examples from the realm of insect--plant interactions.

Invasive species represent one of the most important threats to biodiversity worldwide, with consequences for ecosystem functioning and the delivery of important ecological services to society. Several hypotheses have been generated to explain the success of exotic plants in their new ranges, with escape from their old natural enemies, such as pathogens and herbivores (the ‘enemy release hypothesis’) and novel defensive chemistry (the ‘novel weapons hypothesis’) receiving considerable attention. Thus far, virtually all studies of exotic plants and insects have been conducted in a strictly bi-trophic framework involving plants and herbivores. On the other hand, it has been argued that a better understanding of the forces regulating community structure and function should include natural enemies of the herbivores. Furthermore, indirect interactions between organisms in the plant roots (below-ground) and shoots (above-ground) are known to strongly effect the behaviour and performance of consumers in the opposite ‘compartment’. Here, we discuss a range of physiological, evolutionary and ecological aspects of plant–herbivore-natural enemy interactions involving exotic plants. Further, interactions between soil and above-ground organisms are explored with respect to studies with exotic plants. We argue that it is important to link population and community ecology to individual-level variation in the physiology and behaviour of insects across several trophic levels in studies with invasive plants. Future research with invaders should also aim to integrate physically separated compartments (e.g. plant roots and shoots). This will facilitate a more complete understanding of the factors underlying the success (or failure) of exotic plants to spread and become dominant in their new ranges. Moreover, these data will also help to unravel the relative importance of top-down and bottom-up processes in regulating communities in which exotic plants have become established. Lastly, we discuss consequences for conservation.

Summary 1Plant species employ several direct and indirect defence strategies to protect themselves against insect herbivores. Most studies, however, have focused on shoot-induced responses. Much less is known about interactions between below- and above-ground herbivores and how these may affect their respective parasitoids. 2Here, we quantify the impact of below-ground induced responses vs. that of above-ground induced responses in a feral Brassica on the performance of Pieris brassicae and its endoparasitoid Cotesia glomerata. Jasmonic acid (JA) was applied to induce the plants above- or below-ground. The glucosinolate, sugar and amino acid levels of the leaves were analysed. 3Pieris brassicae larvae grew significantly slower on shoot JA-induced (SJA) plants than on root JA-induced (RJA) and control plants, which were treated with acidic water. On RJA and control plants they showed similar developmental trajectories. Pupal masses, survival till eclosion and egg load, however, were similar on all plants. 4The development of C. glomerata larvae on SJA plants was significantly longer than that on RJA and control plants. In contrast, the parasitoid's pupal stage lasted longer in hosts feeding on control plants. The total developmental times eventually were similar in all groups. However, the masses of male and female C. glomerata adults that developed hosts on control and RJA plants were significantly larger than those from hosts on SJA plants. JA application increased total glucosinolate contents and decreased the sugars and total amino acids levels independent of whether JA was applied. However, the trajectories of herbivore-induced glucosinolate levels differed between RJA and SJA plants. 5These results show that the differential effects of above- and below-ground-induced responses on herbivores also affect higher trophic levels in a nonlinear fashion via differential changes in host plant quality. In particular, the indirect effects that below-ground herbivores have on the performance of above-ground parasitoids may exceed the direct effects of plant chemistry on herbivore performance. Consequently, above-ground and below-ground interactions mediated by induced plant responses have the potential to mediate insect community structure and function in complex ways.

Growing empirical evidence suggests that aboveground and belowground multitrophic communities interact. However, investigations that comprehensively explore the impacts of above- and belowground third and higher trophic level organisms on plant and herbivore performance are thus far lacking. We tested the hypotheses that above- and belowground higher trophic level organisms as well as decomposers affect plant and herbivore performance and that these effects cross the soil-surface boundary. We used a well-validated simulation model that is individual-based for aboveground trophic levels such as shoot herbivores, parasitoids, and hyperparasitoids while considering belowground herbivores and their antagonists at the population level. We simulated greenhouse experiments by removing trophic levels and decomposers from the simulations in a factorial design. Decomposers and above- and belowground third trophic levels affected plant and herbivore mortality, root biomass, and to a lesser extent shoot biomass. We also tested the effect of gradual modifications of the interactions between different trophic level organisms with a sensitivity analysis. Shoot and root biomass were highly sensitive to the impact of the fourth trophic level. We found effects that cross the soil surface, such as aboveground herbivores and parasitoids affecting root biomass and belowground herbivores influencing aboveground herbivore mortality. We conclude that higher trophic level organisms and decomposers can strongly influence plant and herbivore performance. We propose that our modelling framework can be used in future applications to quantitatively explore the possible outcomes of complex above- and belowground multitrophic interactions under a range of environmental conditions and species compositions.

Most studies on plant defenses against insect herbivores investigate direct and indirect plant defenses independently. However, these defenses are not necessarily mutually exclusive. Plant metabolites can be transmitted through the food chain and can also affect the herbivore’s natural enemies. A conflict may arise when a natural enemy is attracted to a plant that is suboptimal in terms of its own fitness. In addition, plant defenses are often studied in cultivated plant species in which artificial selection may have resulted in reduced resistance against insect herbivores. In this study, we investigated both direct and indirect plant defenses in two closely related wild brassicaceous plant species, Brassica nigra L. and Sinapis arvensis L. The herbivore Pieris brassicae L. (Lepidoptera: Pieridae), which is specialized on brassicaceous plant species, developed faster and attained higher pupal mass when reared on B. nigra than on S. arvensis . In contrast, Cotesia glomerata L. (Hymenoptera: Braconidae), which is a gregarious endoparasitoid of P. brassicae caterpillars, developed equally well on P. brassicae irrespective of the food plant on which its host had been reared. The feeding strategy of the parasitoid larvae, that is, selectively feeding on hemolymph and fat body, is likely to allow for a much wider host-size range without affecting the size or development time of the emerging parasitoids. In flight chamber experiments, C. glomerata , which had an oviposition experience in a host that fed on Brussels sprout, exhibited significant preference for host-damaged B. nigra over host-damaged S. arvensis plants. Headspace analysis revealed quantitative and qualitative differences in volatile emissions between the two plant species. This parasitoid species may use a range of cues associated with the host and the host’s food plant in order to recognize the different plant species on which the host can feed. These results show that there is no conflict between direct and indirect plant defenses for this plant‐host‐ parasitoid complex.

Through artificial selection, domesticated plants often contain modified levels of primary and secondary metabolites compared to their wild progenitors. It is hypothesized that the changed chemistry of cultivated plants will affect the performance of insects associated with these plants. In this paper, the development of several specialist and generalist herbivores and their endoparasitoids were compared when reared on a wild and cultivated population of cabbage, Brassica oleracea, and a recently established feral Brassica species. Irrespective of insect species or the degree of dietary specialization, herbivores and parasitoids developed most poorly on the wild population. For the specialists, plant population influenced only development time and adult body mass, whereas for the generalists, plant populations also affected egg-to-adult survival. Two parasitoid species, a generalist (Diadegma fenestrale) and a specialist (D. semiclausum), were reared from the same host (Plutella xylostella). Performance of D. semiclausum was closely linked to that of its host, whereas the correlation between survival of D. fenestrale and host performance was less clear. Plants in the Brassicaceae characteristically produce defense-related glucosinolates (GS). Levels of GS in leaves of undamaged plants were significantly higher in plants from the wild population than from the domesticated populations. Moreover, total GS concentrations increased significantly in wild plants after herbivory, but not in domesticated or feral plants. The results of this study reveal that a cabbage cultivar and plants from a wild cabbage population exhibit significant differences in quality in terms of their effects on the growth and development of insect herbivores and their natural enemies. Although cultivated plants have proved to be model systems in agroecology, we argue that some caution should be applied to evolutionary explanations derived from studies on domesticated plants, unless some knowledge exists on the history of the system under investigation.

Differences in allelochemistry of plants may influence their ability to attract parasitoids.We studied responses of Diadegma semiclausum (Hellén), a parasitoid of the diamondback moth (Plutella xylostella L.), to inter- and intraspecific variation in odor blends of crucifers and a non-crucifer species. Uninfested Brussels sprout (Brassica oleracea L. gemmifera), white mustard (Sinapis alba L.), a feral Brassica oleracea, and malting barley (Hordeum vulgare L.) were compared for their attractivity to D. semiclausum in a Y-tube bioassay. Odors from all plants were more attractive to the parasitoid than clean air. However, tested against each other, parasitoids preferred the volatile blend from the three cruciferous species over that of malting barley.Wasps also discriminated between uninfested crucifers: mustard was as attractive as feral B. oleracea, and both were more attractive than Brussels sprout. Attractivity of uninfested plants was compared with that of plants infested by larvae of the host P. xylostella. Host-infested mustard and Brussels sprout were more attractive than uninfested conspecifics. Interestingly, the volatile blends of uninfested white mustard and infested Brussels sprout were equally attractive.We also compared the volatile composition of different plant sources by collecting headspace samples and analysing them with GC-MS. Similarities of volatile profiles were determined by hierarchic clustering and non-metric scaling based on the Horn-index. Due to the absence of several compounds in its blend, the volatile profile of barley showed dissimilarities from blends of crucifers. The odor profile of white mustard was distinctly different from the two Brassicaceae.Feral Brassica oleracea odor profile was different from infested Brussels sprout, but showed overlap with uninfested Brussels sprout. Odor blends from infested and uninfested Brussels sprout were similar, and mainly quantitative differences were found. D. semiclausum appears to discriminate based on subtle differences in volatile composition of odor blends from infested and uninfested plants. [KEYWORDS: Diadegma semiclausum ; Plutella xylostella ; Hordeum vulgare ; Sinapis alba ; Brassica oleracea ; olfactometer ; headspace volatiles ; GC-MS]

Soil organisms can influence higher trophic level aboveground organisms, but only very few studies have considered such effects. We manipulated soil community composition of model grassland ecosystems by introducing nematode communities, microorganisms, neither or both groups. Above ground, aphids (Rhopalosiphum padi) and parasitoids (Aphidius colemani) were introduced, and we measured individual performance and population dynamics of plants, aphids and parasitoids. In microcosms with nematode inoculations either with or without microorganism inoculation, aphids offspring production was significantly reduced by 31%. Aphid populations on both host plants Agrostis capillaris and Anthoxanthum odoratum were lowest in microcosms with combined nematode and microorganism inoculations. Opposite results were found for parasitoids. While the number of emerged parasitoids did not differ between treatments, parasitoid mortality and the proportion of males were significantly lower in microcosms with nematode and microorganism inoculations. Parasitized aphids were significantly larger in microcosms with nematodes inoculated. Plant biomass did not differ, but in the preferred host plant A. odoratum, foliar phenolic content was reduced in the presence of nematodes, and also the concentration of amino acids in the phloem. This study shows that the composition of the soil community matters for aboveground multitrophic interactions

The capacity of local communities to control introduced plants is called biotic resistance. Biotic resistance has been almost exclusively tested for plant competition and aboveground herbivores and pathogens, while neglecting root herbivores and soil pathogens. Here, we present biotic resistance by above- and belowground herbivores in concert, and relate the abundance of the plant enemies to the species diversity of the local plant communities. The study was carried out in a 7-year-old biodiversity field experiment. We used creeping thistle (Cirsium arvense) as a model, and quantified sap-sucking herbivores: aboveground aphids, their antagonists, and root-feeding nematodes. As plant diversity treatments, we used field plots sown with high (15 plant species, HSD) or low (4 plant species, LSD) diverse seed mixtures in 1996 and that were not weeded. Creeping thistle became established spontaneously at the start of the experiment. In 2002, in HSD plots, 90 % of the plant community was made up by 11 species, compared to seven species in LSD plots. No differences were found for C. arvense abundance or biomass. Aboveground, three aphid species were found on C. arvense-Uroleucon cirsii, Aphis fabae, and Macrosiphum euphorbiae, but the latter was found only in low densities. Significantly more aphid species were found on individual plants in HSD plots. Moreover, in HSD plots, on average 10 % of aphids were parasitized, while no parasitism was observed in LSD plots. In the root zone of C. arvense, significantly more nematodes were found in HSD than in LSD plots, and a significantly higher proportion of those nematodes were plant parasites. The dominant plant parasitic nematode in both treatments was Paratylenchus. We conclude that biotic resistance by natural enemies may be enhanced by plant species diversity, but that above- and belowground sap-sucking herbivores do not necessarily have to respond similarly to the diversity of the surrounding plant community. [KEYWORDS: Aphis fabae ; Macrosiphum euphorbiae ; nematode ; Paratylenchus ; Uroleucon cirsii.]

Plants are frequently attacked by both above- and belowground arthropod herbivores. Nevertheless, studies rarely consider root and shoot herbivory in conjunction. Here we provide evidence that the root-feeding insect Agriotes lineatus reduces the performance of the foliage feeding insect Spodoptera exigua on cotton plants. In a bioassay, S. exigua larvae were allowed to feed on either undamaged plants, or on plants that had previously been exposed to root herbivory, foliar herbivory, or a combination of both. Previous root herbivory reduced the relative growth rates as well as the food consumption of S. exigua by more than 50% in comparison to larvae feeding on the undamaged controls. We found no effects in the opposite direction, as aboveground herbivory by S. exigua did not affect the relative growth rates of root-feeding A. lineatus. Remarkably, neither did the treatment with foliar herbivory affect the food consumption and relative growth rate of S. exigua in the bioassay. However, this treatment did result in a significant change in the distribution of S. exigua feeding. Plants that had been pre-exposed to foliar herbivory suffered significantly less damage on their young terminal leaves. While plant growth and foliar nitrogen levels were not affected by any of the treatments, we did find significant differences between treatments with respect to the level and distribution of plant defensive chemicals (terpenoids). Exposure to root herbivores resulted in an increase in terpenoid levels in both roots as well as in mature and immature foliage. Foliar damage, on the other hand, resulted in high terpenoid levels in young, terminal leaves only. Our results show that root-feeding herbivores may change the level and distribution of plant defenses aboveground. Our data suggest that the reported interactions between below- and aboveground insect herbivores are mediated by induced changes in plant secondary chemistry.

1.The survival of eggs and larvae is dependent on the oviposition site selection of their mothers. In obligate myrmecophilic butterflies, both host plant phenology and host ant presence are expected to affect the decision where to deposit eggs. The importance of ant nest presence in the oviposition site selection of Phengaris butterflies is, however, highly debated.2.We studied oviposition in the largest Phengaris (Maculinea) alcon population in Portugal, exploiting Gentiana pneumonanthe as the host plant and Myrmica aloba as host ant. We collected phenological plant data and recorded the presence and number of eggs on plants with and without Myrmica ants nearby during the flight period of the butterfly.3.Females oviposited on tall plants with many tall buds, while the presence of host ant nests weakly affected oviposition on plants where the probability of finding ants at close range was high. Moreover, larger plants with many tall buds close to host ant nests received more eggs.4.A density-dependent shift in oviposition was not found as the proportion of buds not infected with eggs did not differ between plants with or without ants, whereas plant characteristics did have an effect. Tall plants with many large buds were associated with earlier oviposition.5.Our results suggest that females of P. alcon in Portugal choose gentian plants for oviposition mainly based on plant characteristics whereas the vicinity of ants had a weak effect. Moreover, our study shows that testing the ant-mediated oviposition hypothesis requires baiting ants more than once.

Proximate factors affecting animal behavior include stimuli generated by conspecifics. In spider mites of the genus Tetranychus (Acari: Tetranychidae), males guard pre-reproductive quiescent females, because only the first mating results in fertilization. In a dual-choice experiment, more adult males of T. urticae were attracted to females guarded by a male than to solitary females. Because spider mites are known to perceive volatiles, we hypothesized that guarded and solitary females differ in the volatile blends emitted. To test this hypothesis, headspace volatiles of guarded females, solitary females, and solitary males were collected, respectively. GC/MS analysis detected octanal, methyl salicylate, ethyl 4-ethoxybenzoate, and methyl cis-dihydrojasmonate in all of the groups. Orthogonal Projection to Latent Structures Discriminant Analysis (OPLS-DA) of the blends clearly discriminated guarded females from solitary females, supporting our hypothesis. Individual compounds did not show significant difference in emission rates for guarded females vs. solitary females, suggesting that differences lay in the total blend composition. OPLS-DA did not discriminate between the blends emitted by guarded females and solitary males. In conclusion, the differences in the volatile blends are likely to mediate male discrimination between guarded and solitary females.

Flea beetles are characterized by their tendency to jump. They can also fly. First, the effects of starvation on flight activity in the flea beetle, Phyllotreta nemorum L. (Coleoptera: Chrysomelidae) were determined. After starving P. nemorum for five days a greater number of individuals of both sexes flew than when fed continuously for the same period. In addition, the effect of the mating status of females of P. nemorum on their movement was determined. Mated females were more active than virgin females. It is concluded that starvation stimulates the flight activity of both sexes and mating activates the movement of females of P. nemorum.

Plant secondary metabolites play an important role in mediating interactions with insect herbivores and their natural enemies. Metabolites stored in plant tissues are usually investigated in relation to herbivore behaviour and performance (direct defence), whereas volatile metabolites are often studied in relation to natural enemy attraction (indirect defence). However, so-called direct and indirect defences may also affect the behaviour and performance of the herbivore's natural enemies and the natural enemy's prey or hosts, respectively. This suggests that the distinction between these defence strategies may not be as black and white as is often portrayed in the literature. The ecological costs associated with direct and indirect chemical defence are often poorly understood. Chemical defence traits are often studied in two-species interactions in highly simplified experiments. However, in nature, plants and insects are often engaged in mutualistic interactions with microbes that may also affect plant secondary chemistry. Moreover, plants are challenged by threats above- and belowground and herbivory may have consequences for plant-insect multitrophic interactions in the alternative compartment mediated by changes in plant secondary chemistry. These additional associations further increase the complexity of interaction networks. Consequently, the effect of a putative defence trait may be under- or overestimated when other interactions are not considered.

Over the past two decades a growing body of empirical research has shown that many ecological processes are mediated by a complex array of indirect interactions occurring between rhizosphere-inhabiting organisms and those found on aboveground plant parts. Aboveground–belowground studies have thus far focused on elucidating processes and underlying mechanisms that mediate the behavior and performance of invertebrates in opposite ecosystem compartments. Less is known about genetic variation in plant traits such as defense as that may be driven by above- and belowground trophic interactions. For instance, although our understanding of genetic variation in aboveground plant traits and its effects on community-level interactions is well developed, little is known about the importance of aboveground–belowground interactions in driving this variation. Plant traits may have evolved in response to selection pressures from above- and below-ground interactions from antagonists and mutualists. Here, we discuss gaps in our understanding of genetic variation in plant-related traits as they relate to aboveground and belowground multitrophic interactions. When metabolic resources are limiting, multiple attacks by antagonists in both domains may lead to trade-offs. In nature, these trade-offs may critically depend upon their effects on plant fitness. Natural enemies of herbivores may also influence selection for different traits via top–down control. At larger scales these interactions may generate evolutionary “hotspots” where the expression of various plant traits is the result of strong reciprocal selection via direct and indirect interactions. The role of abiotic factors in driving genetic variation in plant traits is also discussed.

BACKGROUND: Most insect-resistant transgenic crops employ toxins to control pests. A novel approach is to enhance the effectiveness of natural enemies by genetic engineering of the biosynthesis of volatile organic compounds (VOCs). Before the commercialisation of such transgenic plants can be pursued, detailed fundamental studies of their effects on herbivores and their natural enemies are necessary. The linalool/nerolidol synthase gene FaNES1 was constitutively expressed from strawberry in three Arabidopsis thaliana accessions, and the behaviour of the aphid Brevicoryne brassicae L., the parasitoid Diaeretiella rapae McIntosh and the predator Episyrphus balteatus de Geer was studied. RESULTS: Transgenic FaNES1-expressing plants emitted (E)-nerolidol and larger amounts of (E)-DMNT and linalool. Brevicoryne brassicae was repelled by the transgenic lines of two of the accessions, whereas its performance was not affected. Diaeretiella rapae preferred aphid-infested transgenic plants over aphid-infested wild-type plants for two of the accessions. In contrast, female E. balteatus predators did not differentiate between aphid-infested transgenic or wild-type plants. CONCLUSION: The results indicate that the genetic engineering of plants to modify their emission of VOCs holds considerable promise for facilitating biological control of herbivores. Validation for crop plants is a necessary next step to assess the usefulness of modified volatile emission in integrated pest management.

International audience; 1. Belowground herbivory has recently been shown to disrupt the host location behaviour of aboveground parasitoids and thereby impact plants indirect defences. Reverse interactions, on the other hand, have received little attention so far. 2. Lab and field studies were conducted to examine whether the presence of the leaf herbivore Pieris brassicae Linnaeus on brassicaceous plants influences the response of Trybliographa rapae Westwood, a specialist parasitoid of the root feeder Delia radicum Linnaeus. 3. The present results show that the attraction of the parasitoid towards host-infested plants disappeared when these plants were also infested by P. brassicae. This absence of attraction was observed both when the complete odour blend or only undamaged leaves from damaged plants were offered, emphasising the role of systemically induced volatiles for host location in T. rapae. 4. Furthermore, the field study revealed that parasitism levels dropped from 30% on root-infested plants to 4% on double-infested plants. 5. The present study is the first to confirm that reduced attraction to host-infested plants as a result of simultaneous attack by below- and aboveground herbivores translates into lower levels of parasitism in the field.

Flea beetles are characterized by their tendency to jump. They can also fly. First, the effects of starvation on flight activity in the flea beetle, Phyllotreta nemorum L. (Coleoptera: Chrysomelidae) were determined. After starving P. nemorum for five days a greater number of individuals of both sexes flew than when fed continuously for the same period. In addition, the effect of the mating status of females of P. nemorum on their movement was determined. Mated females were more active than virgin females. It is concluded that starvation stimulates the flight activity of both sexes and mating activates the movement of females of P. nemorum.

Trichogramma species (Hymenoptera: Trichogrammatidae) are haplo-diploid egg parasitoids that are frequently used as biological control agents against lepidopteran pests. These wasps display two reproductive modes, including arrhenotoky (bisexuality) and thelytoky (unisexuality). Thelytokous forms are often associated with the presence of endosymbiotic Wolbachia bacteria. The use of thelytokous wasps has long been considered as a way to enhance the efficacy of biological control. The present study investigates the potential of a thelytokous Wolbachia-infected and an arrhenotokous uninfected Trichogramma brassicae Bezdenko strain as inundative biocontrol agents by evaluating their functional response towards different egg densities of the factitious host, the Angoumois grain moth, Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae). The results revealed a type II functional response for both strains in which parasitism efficiency decreases with host egg density because of an increasing host handling time. A model with an indicator variable was used to compare the parameters of Holling's disc equation in different data sets. It was demonstrated that the two strains did not differ in host attack rate. However, the Wolbachia-infected strain did have an increased host handling time when compared to the bisexual strain. Some applied aspects of the findings are discussed.

Root-feeding insects can affect the performance of aboveground insect herbivores when they are forced to feed on the same host plant. Here we explored whether the oviposition behaviour of two closely related herbivorous species (cabbage butterflies; Lepidoptera: Pieridae) is influenced by root-feeding insects, when they are given the chance to choose between host plants with and without root herbivores. Considering that egg load is an important physiological factor influencing the foraging behaviour of insects, we also examined whether root-feeding insects differentially influence oviposition preference in butterflies with low and high egg loads. Oviposition preference in both butterfly species with low and high egg loads was monitored using host plants with and without root herbivores. To ascertain the status of butterfly age with low and high egg loads, the oviducts of a separate group of butterflies was dissected to record the number of immature and mature eggs in butterflies of various ages. Pieris brassicae L. butterflies with low egg loads preferred plants without root herbivores over plants with root herbivores, and laid more egg clutches on the leaves of plants that were not attacked by root herbivores. Butterflies with comparatively high egg loads also selected a larger proportion of plants without root herbivores, but laid a similar number of egg clutches on the plant shoots independent of the presence or absence of root herbivores belowground. Independent of the age and egg load, Pieris rapae L. butterflies selected a larger proportion of plants not attacked by root herbivores to lay eggs, but the number of eggs laid was similar in plants with and without root herbivores. This study shows that belowground insects can influence behavioural decisions of aboveground insect herbivores. Interestingly, the strength of these interactions depends on the physiological state of the insects which is probably correlated with their perception of environmental quality.

Root herbivores and plant mutualists, such as arbuscular mycorrhizal fungi (AMF), have a significant effect on the structure and dynamic of plant communities. Nevertheless, the interactions between the two groups of organisms in natural ecosystems are far from understood. We carried out an inoculation experiment to examine the effect of two root herbivores, Pratylenchus penetrans and P. dunensis (Nematoda), on the composition of the AMF communities associated with two populations of the dune grass Ammophila arenaria. The outcome of the interaction in terms of plant and nematode performance was also analyzed. The total percentage of AMF colonization was not affected by the presence of root-feeders, but they did alter the composition of the AMF communities inside the roots. These changes were dependent on the root-feeder species and the original AMF community: the most severe alterations were observed in the mycorrhizal plants from Wales attacked by P. penetrans. Plant growth was impaired in plants from Wales inoculated with AMF and P. dunensis, which suggests a highly species-specific synergistic interaction with negative consequences for the plant. Root infection by the nematodes was reduced in all mycorrhizal plants when compared to non-mycorrhizal plants. However, a significant reduction of the final number of nematodes was observed only in the mycorrhizal plants from one population. http://www.sciencedirect.com/science/article/B7GVS-4SSP7BN-3/1/fa6c5c650a18615fab2d9cdc479ebf24

Root herbivores can indirectly affect aboveground herbivores by altering the food quality of the plant. However, it is largely unknown whether plant genotypes differ in their response to root herbivores, leading to variable defensive phenotypes. In this study, we investigated whether root-feeding insect larvae (Agriotes sp. larvae, wireworms) induce different responses in Plantago lanceolata plants from lines selected for low and high levels of iridoid glycosides (IG). In the absence of wireworms, plants of the “high-IG line” contained approximately twofold higher levels of total IG and threefold higher levels of catalpol (one of the IG) in leaves than plants from the “low-IG line,” whereas both lines had similar levels of IG in roots. In response to wireworms, roots of plants from both lines showed increased concentrations of catalpol. Leaves of “low-IG line” plants increased catalpol concentrations in response to wireworms, whereas catalpol concentrations of leaves of “high-IG line” plants decreased. In contrast, glucose concentrations in roots of “low-IG” plants decreased, while they increased in “high-IG” plants after feeding by wireworms. The leaf volatile profile differed between the lines, but was not affected by root herbivores. In the field, leaf damage by herbivores was higher in wireworm-induced compared to noninduced “low-IG” plants and lower in wireworm-induced compared to noninduced “high-IG” plants, despite induction of catalpol in leaves of the “low-IG” plants and reduction in “high-IG” plants. This pattern might arise if damage is caused mainly by specialist herbivores for which catalpol may act as feeding stimulant rather than as deterrent. The present study documents for the first time that intraspecific variation in plant defense affects the outcome of plant-mediated interactions between root and shoot herbivores.

Plasmid transfer among isolates of Rhizobium leguminosarum bv. viciae in heavy metal contaminated soils from a long-term experiment in Braunschweig, Germany, was investigated under laboratory conditions. Three replicate samples each of four sterilized soils with total Zn contents of 54, 104, 208 and 340 mg kg −1 were inoculated with an equal number (1×10 5 cells g −1 soil) of seven different, well-characterized isolates of R. leguminosarum bv. viciae . Four of the isolates were from an uncontaminated control plot (total Zn 54 mg kg −1 ) and three were from a metal-contaminated plot (total Zn 340 mg kg −1 ). After 1 year the population size was between 10 6 and 10 7 g −1 soil, and remained at this level in all but the most contaminated soil. In the soil from the most contaminated plot no initial increase in rhizobial numbers was seen, and the population declined after 1 year to −1 soil after 4 years. One isolate originally from uncontaminated soil that had five large plasmids (no. 2-8-27) was the most abundant type re-isolated from all of the soils. Isolates originally from the metal-contaminated soils were only recovered in the most contaminated soil. After 1 year, four isolates with plasmid profiles distinct from those inoculated into the soils were recovered. One isolate in the control soil appeared to have lost a plasmid. Three isolates from heavy metal contaminated soils (one isolate from the soil with total Zn 208 mg kg −1 and two isolates from the soil with total Zn 340 mg kg −1 ) had all acquired one plasmid. Plasmid transfer was confirmed using the distinct ITS–RFLP types of the isolates and DNA hybridization using probes specific to the transferred plasmid. The transconjugant of 2-8-27 which had gained a plasmid was found in one replicate after 2 years of the most contaminated soil but comprised more than 50% of the isolates. A similar type appeared in a separate replicate of the most contaminated soil after 3 years and persisted in both of these soils until the final sampling after 4 years. After 2 years isolates were recovered from four of the soil replicates with the chromosomal type of 2-8-27 which appeared to have lost one plasmid, but these were not recovered subsequently. Isolate 2-8-27 was among the isolates most sensitive to Zn in laboratory assays, whereas isolate 7-13-1 showed greater zinc tolerance. Acquisition of the plasmid conferred enhanced Zn tolerance to the recipients, but transconjugant isolates were not as metal tolerant as 7-13-1, the putative donor. Laboratory matings between 2-8-27 and 7-13-1 in the presence of Zn resulted in the conjugal transfer of the same small plasmid from 7-13-1 to isolate 2-8-27 and the transconjugant had enhanced metal tolerance. Our results show that transfer of naturally-occurring plasmids among rhizobial strains is stimulated by increased metal concentrations in soil. We further demonstrate that the transfer of naturally-occurring plasmids is important in conferring enhanced tolerance to elevated zinc concentrations in rhizobia.

In nature, plants defend themselves by production of allelochemicals that are toxic to herbivores. There may be considerable genetic variation in the expression of chemical defenses because of various selection pressures. In this study, we examined the development of the small cabbage butterfly, Pieris rapae, and its gregarious pupal ectoparasitoid, Pteromalus puparum, when reared on three wild populations (Kimmeridge, Old Harry, Winspit) of cabbage, Brassica oleracea, and a Brussels sprout cultivar. Wild plant populations were obtained from seeds of plants that grow naturally along the south coast of Dorset, England. Significant differences in concentrations of allelochemicals (glucosinolates) were found in leaves of plants damaged by P. rapae. Total glucosinolate concentrations in Winspit plants, the population with the highest total glucosinolate concentration, were approximately four times higher than in the cultivar, the strain with the lowest total glucosinolate concentration. Pupal mass of P. rapae and adult body mass of Pt. puparum were highest when reared on the cultivar and lowest when developing on Kimmeridge plants, the wild strain with the lowest total glucosinolate concentration. Development of male parasitoids was also more negatively affected than female parasitoids. Our results reveal that plant quality, at least for the development of 'adapted' oligophagous herbivores, such as P. rapae, is not based on total glucosinolate content. The only glucosinolate compound that corresponded with the performance of P. rapae was the indole glucosinolate, neoglucobrassicin. Our results show that performance of ectoparasitoids may closely reflect constraints on the development of the host.

It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata, a parasitoid of the leaf herbivore Pieris brassicae, mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.

1. Plants and insects are part of a complex multitrophic environment, in which they closely interact. However, most of the studies have been focused mainly on bi-tritrophic above-ground subsystems, hindering our understanding of the processes that affect multitrophic interactions in a more realistic framework. 2. We studied whether root herbivory by the fly Delia radicum can influence the development of the leaf feeder Pieris brassicae, its parasitoid Cotesia glomerata and its hyperparasitoid Lysibia nana, through changes in primary and secondary plant compounds. 3. In the presence of root herbivory, the development time of the leaf herbivore and the parasitoid significantly increased, and the adult size of the parasitoid and the hyperparasitoid were significantly reduced. The effects were stronger at low root fly densities than at high densities. 4. Higher glucosinolate (sinigrin) levels were recorded in plants exposed to below-ground herbivory, suggesting that the reduced performance of the above-ground insects was via reduced plant quality. Sinigrin contents were highest in plants exposed to low root fly densities, intermediate in plants exposed to high root fly densities and lowest in plants that were not exposed to root herbivory. 5. Our results show, for the first time, that root herbivory via changes in plant quality can reduce the performance of an above-ground multitrophic level food chain. This underlines the importance of integrating a broader range of above- and below-ground organisms to facilitate a better understanding of complex multitrophic interactions and interrelationships. [KEYWORDS: above–below-ground interactions ; Cotesia glomerata ; Lysibia nana ; Pieris brassicae ; plant–insect interactions]

Soil organisms can influence higher trophic level aboveground organisms, but only very few studies have considered such effects. We manipulated soil community composition of model grassland ecosystems by introducing nematode communities, microorganisms, neither or both groups. Above ground, aphids (Rhopalosiphum padi) and parasitoids (Aphidius colemani) were introduced, and we measured individual performance and population dynamics of plants, aphids and parasitoids. In microcosms with nematode inoculations either with or without microorganism inoculation, aphids offspring production was significantly reduced by 31%. Aphid populations on both host plants Agrostis capillaris and Anthoxanthum odoratum were lowest in microcosms with combined nematode and microorganism inoculations. Opposite results were found for parasitoids. While the number of emerged parasitoids did not differ between treatments, parasitoid mortality and the proportion of males were significantly lower in microcosms with nematode and microorganism inoculations. Parasitized aphids were significantly larger in microcosms with nematodes inoculated. Plant biomass did not differ, but in the preferred host plant A. odoratum, foliar phenolic content was reduced in the presence of nematodes, and also the concentration of amino acids in the phloem. This study shows that the composition of the soil community matters for aboveground multitrophic interactions

All terrestrial ecosystems consist of aboveground and belowground components that interact to influence community- and ecosystem-level processes and properties. Here we show how these components are closely interlinked at the community level, reinforced by a greater degree of specificity between plants and soil organisms than has been previously supposed. As such, aboveground and belowground communities can be powerful mutual drivers, with both positive and negative feedbacks. A combined aboveground-belowground approach to community and ecosystem ecology is enhancing our understanding of the regulation and functional significance of biodiversity and of the environmental impacts of human-induced global change phenomena.

In the light of current theories on the effects of intercropping on pest reduction, population responses of the diamondback moth (Plutella xylostella), the cabbage aphid (Brevicoryne brassicae) and the life history traits of the large white butterfly (Pieris brassicae) were studied in a Brussels sprout (Brassica oleracea gemmifera)/malting barley (Hordeum vulgare) additive row intercrop and a Brussels sprout monoculture. More P. xylostella adults were caught in the monoculture than in the intercrop. Numbers of P. xylostella larvae and pupae per sprout plant were lower in intercropped plots than in monocultures. However, more larvae and pupae were found per m2 leaf area in the inter- than in the monocrop. Both the densities per plant and per m2 leaf area of B. brassicae populations were lower in the inter- than in the monocrop. After the barley withered and competition with Brussels sprout abated, aphid densities became higher in the inter- than in the monocrop. These findings may be explained by interspecific plant competition resulting in stressed sprout plants with a smaller size and delayed phenology relative to monocropped plants. Effects of differences in plant nutritional quality on herbivore performance were studied by offering leaves of inter- and monocropped sprout plants to larval P. brassicae. Performance and food utilisation were significantly better on leaves from the intercrop (lower dry weight consumption, higher growth rates) than from the monocrop. Defoliation rate was also higher on leaves of intercropped plants than on monocropped ones. The studies indicate that plant stress and consequent changes in developmental rate and nutritional quality of plants are playing a role in herbivore population responses to intercropping. It is argued that such confounding effects of plant competition in intercropping designs can hamper the evaluation of herbivore responses in pest-suppressive agro-ecosystems. [KEYWORDS: Intercropping; Interspecific competition; "Host plant quality hypothesis"; Brevicoryne brassicae; Plutella xylostella; Pieris brassicae]

Many species of wireworms (larvae of click beetles, Elateridae) are poly- phagous root herbivores. In grasslands under restoration succession with various grass species, we aim to determine the role of wireworms in aboveground vegetation succession. Therefore, it is crucial to know whether wireworms prefer some food plants to others. We have investigated the root preference to different grass species for Agriotes obscurus and Athous haemorrhoidalis and whether these preferences can be explained by covariates. In Experiment 1, individual wireworms could choose between four different plants, one of each species (Anthoxanthum odoratum, Festuca rubra, Holcus lanatus, and Lolium perenne). In Experiment 2, groups of wireworms were released into the soil in the center of 16 plants (4 from each species). We used multinomial logit models (MLMs) to analze the data. In the appendix the use of multinomial response models is clarified with a fictitious example, using the SAS statistic software package. No preference was found in Experiment 1. In Experiment 2 we found differences in attractiveness of plant species depending on wireworm species: A. obscurus preferred grass species from nutrient-rich grasslands (L. perenne and H. lanatus). Both wireworm species disliked F. rubra. The distance from the release point influenced the probability of being found at a certain place at the end of the experiment: wireworms tended to stay in the proximity of the release point. A. haemorrhoidalis was more often found farther from the point of release than A. obscurus. Dispersal was farther from the release point in experiments with young plants (6 weeks) compared to older ones (9 weeks). Results are discussed in a broad ecological context.