Plant and insect cuticular lipids serve as behavioral cues for insects

The roles of plant and insect cuticular lipids in insect and plant interactions are reviewed. Emphasis is given to the influence that the host plant and the surface lipids of the host plant have upon insect herbivores and the predators and parasitoids of these herbivores. Variations in cuticular lipids of herbivorous insects are dependent upon the host plant, and these variations may affect the behavior of predators and parasitoids. The cuticular lipids of species which interact on multiple trophic levels are compared. Similarities were found between the hydrocarbons of herbivorous insects, their host plants, and their predators or parasitoids.     

Contrasting patterns of herbivore and predator pressure on invasive and native plants

Invasive non-native plant species often harbor fewer herbivorous insects than related native plant species. However, little is known about how herbivorous insects on non-native plants are exposed to carnivorous insects, and even less is known on plants that have recently expanded their ranges within continents due to climate warming. In this study we examine the herbivore load (herbivore biomass per plant biomass), predator load (predator biomass per plant biomass) and predator pressure (predator biomass per herbivore biomass) on an inter-continental non-native and an intra-continental range-expanding plant species and two congeneric native species. All four plant species co-occur in riparian habitat in north-western Europe. Insects were collected in early, mid and late summer from three populations of all four species. Before counting and weighing the insects were classified to trophic guild as carnivores (predators), herbivores, and transients. Herbivores were further subdivided into leaf-miners, sap-feeders, chewers and gallers. Total herbivore loads were smaller on inter-continental non-native and intra-continental range-expanding plants than on the congeneric natives. However, the differences depended on time within growing season, as well as on the feeding guild of the herbivore. Although the predator load on non-native plants was not larger than on natives, both non-native plant species had greater predator pressure on the herbivores than the natives. We conclude that both these non-native plant species have better bottom-up as well as top-down control of herbivores, but that effects depend on time within growing season and (for the herbivore load) on herbivore feeding guild. Therefore, when evaluating insects on non-native plants, variation within season and differences among feeding guilds need to be taken into account.     

Intra- and interspecific variation in trophic ecology of ‘predatory’ ants in the subfamily Ponerinae

1. The characterisation of energy flow through communities is a primary goal of ecology. Furthermore, predator–prey interactions can influence both species abundance and community composition. The ant subfamily Ponerinae includes many predatory species that range from generalist insectivores to highly specialised hunters that target a single prey type. Given their high diversity and ubiquity in tropical ecosystems, measuring intra- and interspecific variation in their trophic ecology is essential for understanding the role of ants as predators of insect communities. 2. The stable isotopic composition of nitrogen of 22 species from the ant subfamily Ponerinae was measured, relative to plants and other predatory and herbivorous insects at two Atlantic Forest sites in Argentina. The study tested the general assumption that ponerine ants are all predatory, and examined intra- and interspecific variation in trophic ecology relative to habitat, body size and cytochrome c oxidase subunit 1 sequences (DNA barcoding). 3. Stable isotope analysis revealed that most ponerines occupy high trophic levels (primary and secondary predators), but some species overlapped with known insect herbivores. Species residing at low trophic levels were primarily arboreal and may rely heavily on nectar or other plant-based resources in their diet. In addition, larger species tend to occupy lower trophic positions than smaller species. 4. Although some of the species were divided into two or more genetic clusters by DNA barcoding analysis, these clusters did not correspond to intraspecific variation in trophic position; therefore, colony dietary flexibility most probably explains species that inhabit more than one trophic level.     

Plant genetic differences influence herbivore community structure: evidence from a hybrid willow system

To determine the influence of plant genetic variation on community structure of insect herbivores, we examined the abundances of 14 herbivore species among six genetic classes of willow: Salix eriocephala, S. sericea, their F₁ and F₂ interspecific hybrids, and backcross hybrids to each parental species. We placed 1-year-old plants, grown from seeds generated from controlled crosses, in a common garden. During the growing season, we censused gall-inducing flies and sawflies, leaf-mining insects, and leaf-folding Lepidoptera to determine the community structure of herbivorous insects on the six genetic classes. Our results provided convincing evidence that the community structure of insect herbivores in this hybrid willow system was shaped by genetic differences among the parental species and the hybrid genetic classes. Using MANOVA, we detected significant differences among genetic classes for both absolute and relative abundance of herbivores. Using canonical discriminant analysis, we found that centroid locations describing community structure of the insect herbivores differed for each genetic class. Moreover, the centroids for the four hybrid classes were located well outside of the range between the centroids for the parental species, suggesting that more than additive genetic effects of the two parental species influenced community formation on hybrid classes. Line-cross analysis suggested that plant genetic factors responsible for structuring the herbivore community involved epistatic effects, as well as additive and dominance effects. We discuss the ramifications of these results in regard to the structure of insect herbivore communities on plants and the implications of our findings for the evolution of interspecific interactions.     

Silicon-augmented resistance of plants to herbivorous insects: a review

Silicon (Si) is one of the most abundant elements in the earth's crust, although its essentiality in plant growth is not clearly established. However, the importance of Si as an element that is particularly beneficial for plants under a range of abiotic and biotic stresses is now beyond doubt. This paper reviews progress in exploring the benefits at two‐ and three‐trophic levels and the underlying mechanism of Si in enhancing the resistance of host plants to herbivorous insects. Numerous studies have shown an enhanced resistance of plants to insect herbivores including folivores, borers, and phloem and xylem feeders. Silicon may act directly on insect herbivores leading to a reduction in insect performance and plant damage. Various indirect effects may also be caused, for example, by delaying herbivore establishment and thus an increased chance of exposure to natural enemies, adverse weather events or control measures that target exposed insects. A further indirect effect of Si may be to increase tolerance of plants to abiotic stresses, notably water stress, which can in turn lead to a reduction in insect numbers and plant damage. There are two mechanisms by which Si is likely to increase resistance to herbivore feeding. Increased physical resistance (constitutive), based on solid amorphous silica, has long been considered the major mechanism of Si‐mediated defences of plants, although there is recent evidence for induced physical defence. Physical resistance involves reduced digestibility and/or increased hardness and abrasiveness of plant tissues because of silica deposition, mainly as opaline phytoliths, in various tissues, including epidermal silica cells. Further, there is now evidence that soluble Si is involved in induced chemical defences to insect herbivore attack through the enhanced production of defensive enzymes or possibly the enhanced release of plant volatiles. However, only two studies have tested for the effect of Si on an insect herbivore and third trophic level effects on the herbivore's predators and parasitoids. One study showed no effect of Si on natural enemies, but the methods used were not favourable for the detection of semiochemical‐mediated effects. Work recently commenced in Australia is methodologically and conceptually more advanced and an effect of Si on the plants' ability to generate an induced response by acting at the third trophic level was observed. This paper provides the first overview of Si in insect herbivore resistance studies, and highlights novel, recent hypotheses and findings in this area of research. Finally, we make suggestions for future research efforts in the use of Si to enhance plant resistance to insect herbivores.     

Seasonal and diel variations in the activity of canopy insect herbivores differ between deciduous and evergreen plant species in a tropical dry forest

This study evaluated whether herbivorous insects can be expected to have particular adaptations to withstand the harsh dry season in tropical dry forests (TDFs). We specifically investigated a possible escape in space, with herbivorous insects moving to the few evergreen trees that occur in this ecosystem; and escape in time, with herbivores presenting an increased nocturnal rather than diurnal activity during the dry season. We determined the variation in the free-feeding herbivorous insects (sap-sucking and leaf chewing) between seasons (beginning and middle of both rainy and dry seasons), plant phenological groups (deciduous and evergreen trees) and diel period (diurnal and nocturnal) in a Brazilian TDF. We sampled a total of 5827 insect herbivores in 72 flight-interception traps. Contrary to our expectations, we found a greater herbivore diversity during the dry season, with low species overlap among seasons. In the dry season, evergreen trees supported greater richness and abundance of herbivores as compared to deciduous trees. Insects were also more active at night during the dry season, but no diel differences in insect abundance were detected during the rainy season. These results indicate that the strategies used by insect herbivores to withstand the severe climatic conditions of TDFs during the dry season include both small-scale escape in space and time, with evergreen trees playing a key role in maintaining resident insect herbivore populations in TDFs. Relatively more nocturnal activity during the dry season may be related to the avoidance of harsh climatic conditions during the day. We suggest that the few evergreen tree species occurring in the TDF landscape should be especially targeted for protection in this threatened ecosystem, given their importance for insect conservation.     

Herbivore damage increases avian and ant predation of caterpillars on trees along a complete elevational forest gradient in Papua New Guinea

Signals given off by plants to alert predators to herbivore attack may provide exciting examples of coevolution among organisms from multiple trophic levels. We examined whether signals from mechanically damaged trees (simulating damage by herbivores) attract predators of insects along a complete elevational rainforest gradient in tropical region, where various predators are expected to occur at particular elevational belts. We studied predation of artificial caterpillars on trees with and without ‘herbivorous’ damage; as well as diversity and abundances of potential predators at eight study sites along the elevational gradient (200–3700 m a.s.l.). We focused on attacks by ants and birds, as the main predators of herbivorous insect. The predation rate decreased with elevation from 10% d^?1 at 200 m a.s.l. to 1.8% d^?1 at 3700 m a.s.l. Ants were relatively more important predators in the lowlands, while birds became dominant predators above 1700 m a.s.l. Caterpillars exposed on trees with herbivorous damage were attacked significantly more than caterpillars exposed on trees without damage. Results suggest that relative importance of predators varies along elevational gradient, and that observed predation rates correspond with abundances of predators. Results further show that herbivorous damage attracts both ants and birds, but its effect is stronger for ants.     

Variability in leaf traits,insect herbivory and herbivore performance within and among individuals of four broad-leaved tree species

Individual plants may vary in their suitability as hosts for insect herbivores. The adaptive deme formation hypothesis predicts that this variability will lead to the fine-scale adaptation of herbivorous insects to host individuals. We studied individual and temporal variation in the quality of leaves of the tree species ash, lime, common oak, and sycamore in the field as food for herbivores. We determined herbivore attack and leaf consumption and performance of the generalist caterpillars of Spodoptera littoralis in the laboratory. We further assessed the concentrations of carbon, nitrogen and water in the leaves.All measures of leaf tissue quality varied among and within individuals for all tree species. The level of herbivory differed among the tree individuals in lime, oak and sycamore, but not in ash. Within host individuals, differences in herbivory between the upper and lower crown layer varied in direction and magnitude depending on tree species. In feeding experiments, herbivore performance also varied among and within tree individuals. However, variation in palatability was not consistently related to the leaf traits measured or to herbivory levels in the field. The ranking of individuals with respect to the quality of leaf tissue for herbivorous insects varied between years in lime and oak. Thus, trees of both species might present moving targets for herbivores which prevents fine-scale adaptations. In contrast, among individuals of ash and sycamore the pattern of insect performance remained constant over 2 years. These species may be more suitable hosts for the formation of adapted demes in herbivores.     

Parasitic wasp‐associated symbiont affects plant‐mediated species interactions between herbivores

Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant–insect interactions. Although plant‐associated and herbivore‐associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third‐trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third‐trophic level symbionts act in combination with venom to affect plant‐mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant–insect interactions.     

Predators induce interspecific herbivore competition for food in refuge space

Resource competition among herbivorous arthropods has long been viewed as unimportant because herbivore populations are controlled by predators. Although recently resurrected as an organizing force in arthropod communities on plants, there is still general agreement that resource competition among herbivores is reduced by predators. Here we show the reverse: predators induce interspecific resource competi-tion among herbivores. We found that thrips larvae ( Frankliniella occidentalis ) use the web produced and inhabited by the spider mite Tetranychus urticae as a refuge from predation by the phytoseiid mite Neoseiulus cucumeris . Thrips larvae prefer clean plant parts, but move into the web upon perceiving volatile cues associated with thrips and predators. This behaviour leads to lower predation risk, but also to reduced developmental rate and lower production of thrips larvae due to competition with spider mites. In addition, thrips larvae consume spider-mite eggs. Thus, predators induce interspecific competition and intraguild predation among herbivores within refuge space, even when host plants have an overall green appearance.     

Comparing the plant–herbivore network topology of different insect guilds in Neotropical savannas

1. Herbivorous insects can be classified into several trophic guilds with different levels of specialisation on their host plants, which may influence the topological structure of their trophic networks. The present study tested the hypothesis that the structure of plant–herbivore networks differs between guilds of galling, sucking, and chewing insects. 2. Six areas of Neotropical savannas were studied in two localities in the North of the state of Minas Gerais, Brazil. In each area, interactions between plant and insect species were used to build networks for different guilds. 3. In total, 18 plant–herbivore networks were built, comprising 317 insect morphospecies, 50 plant species, and 489 distinct interactions. The networks were characterised using species richness and different network topological measures (connectance, modularity, nestedness, and specialisation). 4. The results obtained showed no difference in species richness, network size, and connectance between distinct insect herbivore guilds. However, it was found that modularity was higher for exophagous than galling insect networks and nestedness was higher for chewers than for other guilds. On the other hand, galling insect networks showed higher specialisation than exophagous insect networks, and sucking insect networks were more specialised than chewing insect networks. 5. The findings of the present study indicate that, although species richness did not differ between insect guilds of herbivores in Neotropical savannas, the topological structure of networks is sensitive to biological and ecological differences between these herbivore groups. The present study stands out as the first to systematically compare the network structure of different herbivore guilds in Neotropical savannas.     

Explaining Leaf Herbivory Rates on Tree Seedlings in a Malaysian Rain Forest

Seedlings of five species of dipterocarp trees were planted in experimental plots in rain forest gaps in Sabah, Malaysia, and the rates of herbivory on their mature leaves recorded over 6 mo. A novel method was used to estimate the feeding pressure exerted by the local insect herbivore community, derived from the relative abundances of the dominant generalist herbivores and their feeding preferences. Characteristics of the leaves related to their defense and nutritional value were measured—phenolic content, laminar fracture toughness, laminar thickness, and nitrogen content. Three main groups of herbivorous insects were present—coleopteran and lepidopteran herbivores, which were sampled by hand from the seedlings, and orthopteran herbivores, which were sampled by sweep netting. The feeding preferences of the main coleopteran and orthopteran herbivores were determined using laboratory feeding trials. Combining variables in a Principal Components Analysis, a clear separation was found between the five seedling species along the first extracted component. This correlated closely with herbivory rates between species. The first extracted component comprised a negative influence of phenolic content and positive effects of nitrogen content, laminar fracture toughness, abundances of coleopteran and lepidopteran herbivores, and estimated feeding pressure of the coleopteran community. Further studies are required to determine the potential applications of the latter measure of estimated herbivore community impact.     

Effects of variation in Eucalyptus essential oil yield on insect growth and grazing damage

Summary Levels of insect attack and yields of leaf essential oils in Eucalyptus vary widely within and among species. We tested the hypotheses that 1) metabolic cost of oil detoxification increases with increasing oil yield, resulting in lower herbivore growth rates and, consequently, 2) in lower herbivore damage to plants. Distribution of insect damage, eggs, immature insects and adults and feeding rates, growth and survivorship of insects do not support the hypotheses, although a threshold level of oil may be necessary to influence herbivorous insects. Herbivorous beetles tested do not detoxify essential oils. Levels of leaf nitrogen, rather than oil content, explained differences in insect feeding and growth.     

From bottom-up to top-down control of invertebrate herbivores in a retrogressive chronosequence

In the long-term absence of disturbance, ecosystems often enter a decline or retrogressive phase which leads to reductions in primary productivity, plant biomass, nutrient cycling and foliar quality. However, the consequences of ecosystem retrogression for higher trophic levels such as herbivores and predators, are less clear. Using a post-fire forested island-chronosequence across which retrogression occurs, we provide evidence that nutrient availability strongly controls invertebrate herbivore biomass when predators are few, but that there is a switch from bottom-up to top-down control when predators are common. This trophic flip in herbivore control probably arises because invertebrate predators respond to alternative energy channels from the adjacent aquatic matrix, which were independent of terrestrial plant biomass. Our results suggest that effects of nutrient limitation resulting from ecosystem retrogression on trophic cascades are modified by nutrient-independent variation in predator abundance, and this calls for a more holistic approach to trophic ecology to better understand herbivore effects on plant communities.     

Phytophagous insect fauna tracks host plant responses to exotic grass invasion

The high dependence of herbivorous insects on their host plants implies that plant invaders can affect these insects directly, by not providing a suitable habitat, or indirectly, by altering host plant availability. In this study, we sampled Asteraceae flower heads in cerrado remnants with varying levels of exotic grass invasion to evaluate whether invasive grasses have a direct effect on herbivore richness independent of the current disturbance level and host plant richness. By classifying herbivores according to the degree of host plant specialization, we also investigated whether invasive grasses reduce the uniqueness of the herbivorous assemblages. Herbivorous insect richness showed a unimodal relationship with invasive grass cover that was significantly explained only by way of the variation in host plant richness. The same result was found for polyphagous and oligophagous insects, but monophages showed a significant negative response to the intensity of the grass invasion that was independent of host plant richness. Our findings lend support to the hypothesis that the aggregate effect of invasive plants on herbivores tends to mirror the effects of invasive plants on host plants. In addition, exotic plants affect specialist insects differently from generalist insects; thus exotic plants affect not only the size but also the structural profile of herbivorous insect assemblages.     

Indirect effect of aquatic insect emergence on a terrestrial insect population through by birds predation

A manipulative field experiment was performed to determine the effect of birds, subsidized by aquatic insect emergence, on the insect herbivores in a riparian deciduous forest. Insectivorous birds were observed more frequently in the riparian forest than in upland forest away from the stream, utilizing both herbivorous insects feeding on the riparian vegetation and aquatic insects emerging from the stream as their prey. Field experiments revealed that the insect herbivore population in the riparian forest was more depressed by bird predation than that in the upland forest. This suggests that allochthonous prey input to the in situ prey population was responsible for a modification in the interaction between birds and herbivorous insects, resulting in a heterogeneous food web structure in the forest.     

Detritivory: stoichiometry of a neglected trophic level

Previous syntheses have identified the key roles that phylogeny, body size, and trophic level play in determining arthropod stoichiometry. To date, however, detritivores have been largely omitted from such syntheses, despite their importance in nutrient cycling, biodiversity, and food web interactions. Here, we report on a compiled database of the allometry and nutritional stoichiometry (N and P) of detritivorous arthropods. Overall, both N and P content for detritivores varied among major phylogenetic lineages. Detritivore N content was similar to the N content of herbivores, but below that of predators. By contrast, detritivore P content was independent of trophic level. Contrary to previous reports, neither nutrient varied with body size. This analysis places detritivores in the context of related herbivores and predators, and as such, sets the stage for future investigations into the causes and consequences of elemental (mis)matches between detritivores and their detrital resources. Holly M. Martinson and Katie Schneider are co-first author.     

Predator Presence Moves <Emphasis Type="Italic">Helicoverpa armigera</Emphasis> Larvae to Distraction

Displacement of herbivorous insects by the presence of predators on whole plants has rarely been studied. By semi-continuous observations of an externally feeding insect herbivore and a predator, we show how the mere presence of the predator, Geocoris lubra Kirkaldy (Hemiptera: Geocoridae), on a plant can have a strong influence on the movement and behaviors of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) larvae. The presence of predators, as opposed to mortality by predators, influenced the proportion of larvae feeding, resting and implementing avoidance activities. In addition, the proportion of time individual larvae allocated to feeding, resting and dropping off plants was affected when predators were present with and without contact between the two. Predators do more than just reduce numbers of herbivores; they influence feeding, displacement and subsequently the distribution of plant damage.     

Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals

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.     

Ecological and Evolutionary Interactions between Wild Crucifers and Their Herbivorous Insects

Abstract Insects feeding on ten species of wild crucifer were investigated. Differences in host plant range and insect community structure were examined with regard to anti-herbivore defense mechanisms. Most of the crucifer species deterred insect herbivory by disappearing in the summer or by lowering their intrinsic quality as food for insects. Species with these defense mechanisms were exploited by only a few specialized herbivorous insects that seemed to have counter defenses. The plants without these defense mechanisms were used by many herbivorous insect species. Rorippa indica lacked direct defenses, but supported a low total density of herbivore individuals. This crucifer has an indirect defense mechanism: ants attracted to floral nectar defended the plant from deleterious herbivores. Crucifers that disappeared seasonally lacked other anti-herbivore defense mechanisms. This suggests that the phonological response is an alternative other responses to herbivore attack.