Insect-resistant transgenic plants in a multi-trophic context

So far, genetic engineering of plants in the context of insect pest control has involved insertion of genes that code for toxins, and may be characterized as the incorporation of biopesticides into classical plant breeding. In the context of pesticide usage in pest control, natural enemies of herbivores have received increasing attention, because carnivorous arthropods are an important component of insect pest control. However, in plant breeding programmes, natural enemies of herbivores have largely been ignored, although there are many examples that show that plant breeding affects the effectiveness of biological control. Negative influences of modified plant characteristics on carnivorous arthropods may induce population growth of new, even more harmful pest species that had no pest status prior to the pesticide treatment. Sustainable pest management will only be possible when negative effects on non-target, beneficial arthropods are minimized. In this review, we summarize the effects of insect-resistant crops and insect-resistant transgenic crops, especially Bt crops, from a food web perspective. As food web components, we distinguish target herbivores, non-target herbivores, pollinators, parasitoids and predators. Below-ground organisms such as Collembola, nematodes and earthworms should also be included in risk assessment studies, but have received little attention. The toxins produced in Bt plants retain their toxicity when bound to the soil, so accumulation of these toxins is likely to occur. Earthworms ingest the bound toxins but are not affected by them. However, earthworms may function as intermediaries through which the toxins are passed on to other trophic levels. In studies where effects of insect-resistant (Bt) plants on natural enemies were considered, positive, negative and no effects have been found. So far, most studies have concentrated on natural enemies of target herbivores. However, Bt toxins are structurally rearranged when they bind to midgut receptors, so that they are likely to lose their toxicity inside target herbivores. What happens to the toxins in non-target herbivores, and whether these herbivores may act as intermediaries through which the toxins may be passed on to the natural enemies, remains to be studied.     

Parasitoids follow herbivorous insects to a novel host plant,generalist predators less so

The ‘enemy‐free space’ hypothesis predicts that herbivorous insects can escape their natural enemies by switching to a novel host plant, with consequences for the evolution of host plant specialisation. However, if natural enemies follow herbivores to their novel host plants, enemy‐free space may only be temporary. We tested this by studying the colonisation of the introduced tree Eucalyptus grandis (Hill) Maiden (Myrtaceae) by insects in Brazil, where various species of herbivores have added eucalyptus to their host plant range, which consists of native myrtaceous species such as guava. Some herbivores, for example, Thyrinteina leucoceraea Ringe (Lepidoptera: Geometridae), cause outbreaks in eucalyptus plantations but not on guava, possibly because eucalyptus offers enemy‐free space. We sampled herbivores (mainly Lepidoptera species) and natural enemies on eucalyptus and guava and assessed parasitism of Lepidoptera larvae on both host plant species during ca. 2 years. Overall, predators were encountered more frequently on guava than on eucalyptus. In contrast, parasitoids were encountered equally and parasitism rates of Lepidoptera larvae were similar on both host plants. This indicates that herbivores may escape some enemies by moving to a novel host plant. However, this escape may be temporary and may vary with time. We argue that studying temporal and spatial patterns of enemy‐free space and the response of natural enemies to host use changes of their herbivorous prey is essential for understanding the role of natural enemies in the evolution of host plant use by herbivorous arthropods.     

Plant composition,not richness,drives occurrence of specialist herbivores

1. How herbivore plant diversity relationships are shaped by the interplay of biotic and abiotic environmental variables is only partly understood. For instance, plant diversity is commonly assumed to determine abundance and richness of associated specialist herbivores. However, this relationship can be altered when environmental variables such as temperature covary with plant diversity. 2. Using gall‐inducing arthropods as focal organisms, biotic and abiotic environmental variables were tested for their relevance to specialist herbivores and their relationship to host plants. In particular, the hypothesis that abundance and richness of gall‐inducing arthropods increase with plant richness was addressed. Additionally, the study asked whether communities of gall‐inducing arthropods match the communities of their host plants. 3. Neither abundance nor species richness of gall‐inducing arthropods was correlated with plant richness or any other of the tested environmental variables. Instead, the number of gall species found per plant decreased with plant richness. This indicates that processes of associational resistance may explain the specialised plant herbivore relationship in our study. 4. Community composition of gall‐inducing arthropods matched host plant communities. In specialised plant herbivore relationships, the presence of obligate host plant species is a prerequisite for the occurrence of its herbivores. 5. It is concluded that the abiotic environment may only play an indirect role in shaping specialist herbivore communities. Instead, the occurrence of specialist herbivore communities might be best explained by plant species composition. Thus, plant species identity should be considered when aiming to understand the processes that shape diversity patterns of specialist herbivores.     

The Effect of Host-Plant Phylogenetic Isolation on Species Richness,Composition and Specialization of Insect Herbivores: A Comparison between Native and Exotic Hosts

Understanding the drivers of plant-insect interactions is still a key issue in terrestrial ecology. Here, we used 30 well-defined plant-herbivore assemblages to assess the effects of host plant phylogenetic isolation and origin (native vs. exotic) on the species richness, composition and specialization of the insect herbivore fauna on co-occurring plant species. We also tested for differences in such effects between assemblages composed exclusively of exophagous and endophagous herbivores. We found a consistent negative effect of the phylogenetic isolation of host plants on the richness, similarity and specialization of their insect herbivore faunas. Notably, except for Jaccard dissimilarity, the effect of phylogenetic isolation on the insect herbivore faunas did not vary between native and exotic plants. Our findings show that the phylogenetic isolation of host plants is a key factor that influences the richness, composition and specialization of their local herbivore faunas, regardless of the host plant origin.     

Compensation behaviour by insect herbivores and natural enemies: its influence on community structure

Insect herbivores feeding on low-quality plants often compensate by increasing their consumption of plant tissue. This usually results in a longer developmental time leading to a higher vulnerability to natural enemies. This has been termed the slow-growth, high-mortality hypothesis. To explore how compensation may shape the species composition of herbivore and natural enemy populations, we present a mathematical model of a tri-trophic system incorporating both the nutritional quality of plants and herbivores, and the compensatory ability of herbivores and their natural enemies. Using this model we predict the abundance of herbivores and natural enemies, and some characteristics of the composition of species of insect communities along a gradient of plant nutritional quality. Specifically, we make the following predictions: 1) In the absence of natural enemies, the abundance of the juvenile herbivores increases with plant quality, and only highly compensating herbivores persist at low plant nutritional quality. 2) If natural enemies are present, the abundance of the juvenile herbivores decreases with increasing plant quality due to more effective suppression by the natural enemies. Poorly compensating herbivores increase while their highly compensating counterparts decrease with lowered plant quality. 3) When the plants have low nutritional quality, natural enemies will only persist when either very highly compensating herbivores are present or if the natural enemy itself is highly compensating. 4) The abundance of adult herbivores in a community with natural enemies can either increase or decrease with increasing plant quality depending on the compensatory abilities of herbivores and natural enemies.     

Do alien plants escape from natural enemies of congeneric residents? Yes but not from all

As predicted by the enemy release hypothesis, plants are supposedly less attacked by herbivores in their introduced range than in their native range. However, the nature of the natural enemies, in particular their degree of specificity may also affect the level of enemy escape. It is therefore expected that ectophagous invertebrate species, being generally considered as more generalists than endophagous species, are more prompt to colonise alien plants. In Swiss, Siberian and Russian Far East arboreta, we tested whether alien woody plants are less attacked by native herbivorous insects than native congeneric woody plant species. We also tested the hypothesis that leaf miners and gall makers show stronger preference for native woody plants than external leaf chewers. In all investigated regions, leaf miners and gall makers were more abundant and showed higher species richness on native woody plants than on congeneric alien plants. In contrast, external leaf chewers did not cause more damage to native plants than to alien plants, possibly because leaf chewers are, in general, less species specific than leaf miners and gall makers. These results, obtained over a very large number of plant-enemy systems, generally support the hypothesis that alien plants partly escape from phytophagous invertebrates but also show that different feeding guilds may react differently to the introduction of alien plants.     

Species richness of Macrolepidoptera on Finnish deciduous trees and shrubs

Summary Species richness of Macrolepidoptera on Finnish trees and shrubs was analysed by means of stepwise regression analysis. The explaining variables were plant frequency, geographical range, plant height, number of relatives and leaf size.Total frequency of the host plant, which correlated strongly with range, explained 57% of the observed variance of lepidopteran species richness on deciduous trees and shrubs. Height of plant and number of relatives explained significantly the residual variation and altogether these three variables explained 71% of the variance of species richness.Analyses at the plant genus level gave similar results and frequency, height and number of relatives explained 78% of the variance of species richness of Macrolepidoptera on deciduous plant genera.When conifers were included in the analysis leaf size also becomes a significant variable. Leaf size can, however, act as a dummy variable which effectively distinguishes conifers from deciduous trees.The validity of different models explaining herbivore species richness on plants is discussed. The results of this study favoured more than earlier studies the importance of relatedness of host plants as a factor which determines the species richness of herbivores.     

Herbivores,saprovores and natural enemies respond differently to within-field plant characteristics of wheat fields

Understanding ecosystem functioning in a farmland context by considering the variety of ecological strategies employed by arthropods is a core challenge in ecology and conservation science. We adopted a functional approach in an assessment of the relationship between three functional plant groups (grasses, broad-leaves and legumes) and the arthropod community in winter wheat fields in a Mediterranean dryland context. We sampled the arthropod community as thoroughly as possible with a combination of suction catching and flight-interception trapping. All specimens were identified to the appropriate taxonomic level (family, genus or species) and classified according to their form of feeding: chewing-herbivores, sucking-herbivores, flower-consumers, omnivores, saprovores, parasitoids or predators. We found, a richer plant community favoured a greater diversity of herbivores and, in turn, a richness of herbivores and saprovores enhanced the communities of their natural enemies, which supports the classical trophic structure hypothesis. Grass cover had a positive effect on sucking-herbivores, saprovores and their natural enemies and is probably due to grasses’ ability to provide, either directly or indirectly, alternative resources or simply by offering better environmental conditions. By including legumes in agroecosystems we can improve the conservation of beneficial arthropods like predators or parasitoids, and enhance the provision of ecosystem services such as natural pest control.     

Predicting the effects of climate change on natural enemies of agricultural pests

Climate change can have diverse effects on natural enemies of pest species. Here we review these effects and their likely impacts on pest control. The fitness of natural enemies can be altered in response to changes in herbivore quality and size induced by temperature and CO₂ effects on plants. The susceptibility of herbivores to predation and parasitism could be decreased through the production of additional plant foliage or altered timing of herbivore life cycles in response to plant phenological changes. The effectiveness of natural enemies in controlling pests will decrease if pest distributions shift into regions outside the distribution of their natural enemies, although a new community of enemies might then provide some level of control. As well as being affected by climate through host plants and associated herbivores, the abundance and activity of natural enemies will be altered through adaptive management strategies adopted by farmers to cope with climate change. These strategies may lead to a mismatch between pests and enemies in space and time, decreasing their effectiveness for biocontrol. Because of the diverse and often indirect effects of climate change on natural enemies, predictions will be difficult unless there is a good understanding of the way environmental effects impact on tritrophic interactions. In addition, evolutionary changes in both hosts and natural enemies might have unexpected consequences on levels of biocontrol exerted by enemies. We consider interactions between the pest light brown apple moth and its natural enemies to illustrate the type of data that needs to be collected to make useful predictions.     

Non-native plants rarely provide suitable habitat for native gall-inducing species

For insect herbivores, a critical niche requirement—possibly the critical niche requirement—is the presence of suitable host plants. Current research suggests that non-native plants are not as suitable as native plants for native herbivores, resulting in decreases in insect abundance and richness on non-native plants. Like herbivores, gall-forming insects engage in complex, species-specific interactions with host plants. Galls are plant tissue tumors (including bulbous or spindle-shaped protrusions on leaves, stems and other plant organs) that are induced by insects through physical or chemical damage (prompting plants to grow a protective tissue shell around the insect eggs and larvae). As such, we hypothesized that gall-inducing insect species richness would be higher on native than non-native plants. We also predicted higher gall-inducing insect species richness on woody than herbaceous plants. We used an extensive literature review in which we compiled gall host plant species by genus, and we assigned native or non-native (or mixed) status to each genus. We found that native plants host far more gall-inducing insect species than non-native plants; woody plants host more gall-inducing species than herbaceous plants; and native woody plants host the most gall-inducing species of all. Gall-inducing species generally are a very cryptic group, even for experts, and hence do not elicit the conservation efforts of more charismatic insects such as plant pollinators. Our results suggest that non-native plants, particularly non-native woody species, diminish suitable habitat for gall-inducing species in parallel with similar results found for other herbivores, such as Lepidopterans. Hence, the landscape-level replacement of native with non-native species, particularly woody ones, degrades taxonomically diverse gall-inducing species (and their inquilines and parasitoids), removing multiple layers of diversity from forest ecosystems.

     

Experimental plant invasion reduces arthropod abundance and richness across multiple trophic levels

Plant invasions are known to have negative impacts on native plant communities, yet their influence on higher trophic levels has not been well documented. Past studies investigating the effects of invasive plants on herbivores and carnivores have been largely observational in nature and thus lack the ability to tease apart whether differences are a cause or consequence of the invasion. In addition, understanding how plant traits and plant species compositions change in invaded habitats may increase our ability to predict when and where invasive plants will have effects that cascade to animals. To assess effects on arthropods, we experimentally introduced a non‐native plant (Microstegium vimineum, Japanese stiltgrass) in a community re‐assembly experiment. We also investigated possible mechanisms through which the invader could affect associated arthropods, including changes in native plant species richness, above‐ground plant biomass, light availability and vegetation height. In experimentally invaded plots, arthropod abundance was reduced by 39%, and species richness declined by 19%. Carnivores experienced greater reductions in abundance than herbivores (61% vs 31% reduction). Arthropod composition significantly diverged between experimentally invaded and control plots, and particular species belonging to the abundant families Aphididae (aphids), Formicidae (ants) and Phalacridae (shining flower beetles) contributed the most to compositional differences. Among the mechanisms we investigated, only the reduction in native plant species richness caused by invasion was strongly correlated with total arthropod abundance and richness. In sum, our results demonstrate negative impacts of M. vimineum invasion on higher trophic levels and suggest that these effects occur, in part, indirectly through invader‐mediated reductions in the richness of the native plant community. The particularly strong response of carnivores suggests that plant invasion could reduce top–down control of herbivorous species for native plants.     

Cascade effects of crop species richness on the diversity of pest insects and their natural enemies

Understanding how plant species richness influences the diversity of herbivorous and predatory/parasitic arthropods is central to community ecology.We explore the effects of crop species richness on the diversity of pest insects and their natural enemies.Using data from a four-year experiment with five levels of crop species richness,we found that crop species richness significantly affected the pest species richness,but there were no significant effects on richness of the pests’natural enemies.In contrast,the species richness of pest insects significantly affected their natural enemies.These findings suggest a cascade effect where trophic interactions are strong between adjacent trophic levels,while the interactions between connected but nonadjacent trophic levels are weakened by the intermediate trophic level.High crop species richness resulted in a more stable arthropod community compared with communities in monoculture crops.Our results highlight the complicated cross-trophic interactions and the crucial role of crop diversity in the food webs of agro-ecosystems.     

When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses

Two venerable hypotheses, widely cited as explanations for either the success or failure of introduced species in recipient communities, are the natural enemies hypothesis and the biotic resistance hypothesis. The natural enemies hypothesis posits that introduced organisms spread rapidly because they are liberated from their co‐evolved predators, pathogens and herbivores. The biotic resistance hypothesis asserts that introduced species often fail to invade communities because strong biotic interactions with native species hinder their establishment and spread. We reviewed the evidence for both of these hypotheses as they relate to the importance of non‐domesticated herbivores in affecting the success or failure of plant invasion.
To evaluate the natural enemies hypothesis, one must determine how commonly native herbivores have population‐level impacts on native plants. If native herbivores seldom limit native plant abundance, then there is little reason to think that introduced plants benefit from escape from these enemies. Studies of native herbivore‐native plant interactions reveal that plant life‐history greatly mediates the strength with which specialist herbivores suppress plant abundance. Relatively short‐lived plants that rely on current seed production for regeneration are most vulnerable to herbivory that reduces seed production. As such, these plants may gain the greatest advantage from escaping their specialist enemies in recipient communities. In contrast, native plants that are long lived or that possess long‐lived seedbanks may not be kept “in check” by native herbivores. For these species, escape from native enemies may have little to do with their success as exotics; they are abundant both where they are native and introduced.
Evidence for native herbivores providing biotic resistance to invasion by exotics is conflicting. Our review reveals that: 1) introduced plants can attract a diverse assemblage of native herbivores and that 2) native herbivores can reduce introduced plant growth, seed set and survival. However, the generality of these impacts is unclear, and evidence that herbivory actually limits or reduces introduced plant spread is scarce. The degree to which native herbivores provide biotic resistance to either exotic plant establishment or spread may be greatly determined by their functional and numerical responses to exotic plants, which we know little about. Generalist herbivores, through their direct effects on seed dispersal and their indirect effects in altering the outcome of native–non‐native plant competitive interactions, may have more of a facilitative than negative effect on exotic plant abundance.     

Insect diversity in the Cape Floristic Region

The Cape Floristic Region (CFR) is characterized by exceptionally high plant species richness and it is yet to be determined whether this is matched by an equally high diversity of insect fauna associated with these plants. In an attempt to do this, data from the literature on the number of insects for various taxa found at different sites in the CFR were compared with equivalent data from other areas in South Africa and elsewhere. Results indicate that the herbivorous insect fauna of the CFR is not particularly rich in species, perhaps except for the small guild of endophagous insects. It is speculated that this is the result of CFR vegetation being a poor food source for herbivores, particularly in view of its sclerophyllous nature. Plant defence mechanisms, such as a pronounced cyanogenic ability of the leaves coupled with the relatively simple architecture of the plants are possible contributing factors.     

Attractiveness of Michigan native plants to arthropod natural enemies and herbivores

The use of plants to provide nectar and pollen resources to natural enemies through habitat management is a growing focus of conservation biological control. Current guidelines frequently recommend use of annual plants exotic to the management area, but native perennial plants are likely to provide similar resources and may have several advantages over exotics. We compared a set of 43 native Michigan perennial plants and 5 frequently recommended exotic annual plants for their attractiveness to natural enemies and herbivores for 2 yr. Plant species differed significantly in their attractiveness to natural enemies. In year 1, the exotic annual plants outperformed many of the newly established native perennial plants. In year 2, however, many native perennial plants attracted higher numbers of natural enemies than exotic plants. In year 2, we compared each flowering plant against the background vegetation (grass) for their attractiveness to natural enemies and herbivores. Screening individual plant species allowed rapid assessment of attractiveness to natural enemies. We identified 24 native perennial plants that attracted high numbers of natural enemies with promise for habitat management. Among the most attractive are Eupatorium perfoliatum L., Monarda punctata L., Silphium perfoliatum L., Potentilla fruticosa auct. non L., Coreopsis lanceolata L., Spiraea alba Duroi, Agastache nepetoides (L.) Kuntze, Anemone canadensis L., and Angelica atropurpurea L. Subsets of these plants can now be tested to develop a community of native plant species that attracts diverse natural enemy taxa and provides nectar and pollen throughout the growing season.     

Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks

In response to feeding by phytophagous arthropods, plants emit volatile chemicals. This is shown to be an active physiological response of the plant and the released chemicals are therefore called herbivore-induced plant volatiles (HIPV). One of the supposed functions of HIPV for the plant is to attract carnivorous natural enemies of herbivores. Depending on which plant and herbivore species interact, blends of HIPV show qualitative and quantitative variation. Hence, one may ask whether this allows the natural enemies to discriminate between volatiles from plants infested by herbivore species that are either suitable or unsuitable as a food source for the natural enemy. Another question is whether natural enemies can also recognise HIPV when two or more herbivore species that differ in suitability as a food source simultaneously attack the same plant species. By reviewing the literature we show that arthropod predators and parasitoids can tell different HIPV blends apart in several cases of single plant–single herbivore systems and even in single plant–multiple herbivore systems. Yet, there are also cases where predators and parasitoids do not discriminate or discriminate only after having learned the association between HIPV and herbivores that are either suitable or non-suitable as a source of food. In this case, suitable herbivores may profit from colonising plants that are already infested by another non-suitable herbivore. The resulting temporal or partial refuge may have important population dynamical consequences, as such refuges have been shown to stabilise otherwise unstable predator–prey models of the Lotka-Volterra or Nicholson-Bailey type.     

Herbivore induced plant volatiles: Their role in plant defense for pest management

Plants respond to herbivory through different defensive mechanisms. The induction of volatile emission is one of the important and immediate response of plants to herbivory. Herbivore-induced plant volatiles (HIPVs) are involved in plant communication with natural enemies of the insect herbivores, neighboring plants, and different parts of the damaged plant. Release of a wide variety of HIPVs in response to herbivore damage and their role in plant-plant, plant-carnivore and intraplant communications represents a new facet of the complex interactions among different trophic levels. HIPVs are released from leaves, flowers, and fruits into the atmosphere or into the soil from roots in response to herbivore attack. Moreover, HIPVs act as feeding and/or oviposition deterrents to insect pests. HIPVs also mediate the interactions between the plants and the microorganisms. This review presents an overview of HIPVs emitted by plants, their role in plant defense against herbivores and their implications for pest management.     

Ant associations in the Neotropical shrub Turnera subulata (Turneraceae): Costs or benefits to the host plant?

The results of ecological interactions depend on the costs and benefits involved in different ecological contexts. Turnera subulata is a shrubby plant with extrafloral nectaries that are associated with ants. Here, we test the hypotheses that the association between T. subulata and ants results in: (i) positive effects on host plant growth and reproduction; (ii) plant herbivory reduction and (iii) inhibition of the host plant visitation by beneficial organisms. Thirty experimental plots were established in northeastern Brazil, either in association with ants or without ants (N = 15 plots/treatment), with four plants each (total 120 plants). Vegetative growth (plant height and number of leaves), reproductive investment (flowers and fruits), herbivory rates and numbers of beneficial visitors were quantified during all phenological stages of the host plant. Data were analysed using generalized linear mixed models. At the host plant maturation stage, we found a trade‐off between growth and reproduction. Plants with ants had lower mean height; however, they invested more in reproduction (a higher number of flowers and fruits) compared to plants without ants. During the flowering stage, the abundance of sucking herbivores was higher in plots without ants but chewing herbivore abundance increased in the maturation stage in plots with ants. The cumulative proportion of leaves with herbivore damage did not differ between treatments, and the presence of ants reduced the number of beneficial visitors (e.g. pollinators and natural enemies) to the host plants. Our results show that association with ants results in some costs for the host plant, however, these costs appear to be offset by the defensive role of ants, which favours plant reproductive investment. In general, our results help to elucidate mechanisms involved in trophic interactions within the complex network of interactions involving ants and plants.     

Comparison of pollinators and natural enemies: a meta‐analysis of landscape and local effects on abundance and richness in crops

To manage agroecosystems for multiple ecosystem services, we need to know whether the management of one service has positive, negative, or no effects on other services. We do not yet have data on the interactions between pollination and pest‐control services. However, we do have data on the distributions of pollinators and natural enemies in agroecosystems. Therefore, we compared these two groups of ecosystem service providers, to see if the management of farms and agricultural landscapes might have similar effects on the abundance and richness of both. In a meta‐analysis, we compared 46 studies that sampled bees, predatory beetles, parasitic wasps, and spiders in fields, orchards, or vineyards of food crops. These studies used the proximity or proportion of non‐crop or natural habitats in the landscapes surrounding these crops (a measure of landscape complexity), or the proximity or diversity of non‐crop plants in the margins of these crops (a measure of local complexity), to explain the abundance or richness of these beneficial arthropods. Compositional complexity at both landscape and local scales had positive effects on both pollinators and natural enemies, but different effects on different taxa. Effects on bees and spiders were significantly positive, but effects on parasitoids and predatory beetles (mostly Carabidae and Staphylinidae) were inconclusive. Landscape complexity had significantly stronger effects on bees than it did on predatory beetles and significantly stronger effects in non‐woody rather than in woody crops. Effects on richness were significantly stronger than effects on abundance, but possibly only for spiders. This abundance‐richness difference might be caused by differences between generalists and specialists, or between arthropods that depend on non‐crop habitats (ecotone species and dispersers) and those that do not (cultural species). We call this the ‘specialist‐generalist’ or ‘cultural difference’ mechanism. If complexity has stronger effects on richness than abundance, it might have stronger effects on the stability than the magnitude of these arthropod‐mediated ecosystem services. We conclude that some pollinators and natural enemies seem to have compatible responses to complexity, and it might be possible to manage agroecosystems for the benefit of both. However, too few studies have compared the two, and so we cannot yet conclude that there are no negative interactions between pollinators and natural enemies, and no trade‐offs between pollination and pest‐control services. Therefore, we suggest a framework for future research to bridge these gaps in our knowledge.     

Effects of spontaneous field margin vegetation on the regulation of herbivores in two winter crops

Non-crop vegetation of field margins provides resources for natural enemies of crop herbivores. However, it is still not well known whether this resource provisioning effect is strong enough to improve herbivore regulation within crop fields and which plant species and functional groups favour this ecosystem service. A better understanding of the interactions between field margin vegetation and herbivore regulation is crucial to evaluate management strategies and to design suppressive plant mixtures. We surveyed 64 wheat and oilseed rape fields of Western France for two years (16 fields per year and crop) in order (1) to identify plant diversity or group effects on herbivore regulation within crop fields and (2) to identify species within plant groups that improve regulation. Herbivores, herbivore damage and natural enemies were monitored on crop plants at a distance of 5 and 50 m from the field margin. At the same time, the cover and phenological stage of all vascular plants were estimated in the adjacent field margin. The study demonstrated a positive relationship between the cover of entomophilous plant species that were flowering at the survey date and response variables related to herbivore regulation. Plant species richness and the cover of plant species taxonomically close to crop plants had a small influence on herbivores and natural enemies in wheat whereas related wild Brassicaceae increased herbivory and decreased herbivore regulation in oilseed rape. Within the entomophilous flowering plants, several species were significantly related to a better herbivore regulation in univariate analyses. Multivariate ordination techniques allowed the identification of plant species influencing several response variables of herbivore regulation at the same time. Our study demonstrated the importance of entomophilous species that flowered at peak infestation of crop herbivores. Spontaneous field margins rich in flowering entomophilous species provide an important ecosystem service without expensive sowing of seed mixtures.