Evolution of plant volatile production in insect-plant relationships

Summary The production of volatile secondary plant substances during the evolution of terrestrial plants is reviewed in regard to the defensive systems of plants to microorganisms and herbivores. Plant volatiles can be produced by both anabolic and catabolic processes. Although attraction of pollinators is a well-studied phenomenon, functions of volatiles range from excretion of waste products to the production of compounds attracting natural enemies of herbivores. During the evolution of the angiosperms a diversity of volatiles were selected to defend generative parts against microorganisms. Many of these allomones were related to or even identical with sex pheromones of insects. As a result flowers of angiosperms became utilized as a mating site. Consequently insects visiting flowers became involved in pollination, facilitating the steps from anemophily to entomophily. The efficiency of entomophily was increased because of nutritional rewards.An evolutionary scenario for the impact of plant volatiles on insects is presented and the role of volatile allomones in the establishment of plant-insect relationships is emphasized by (1) their strong antimicrobial properties, (2) strategies to protect symbiotic microorganisms, (3) their function as repellents and deterrents, (4) the use of volatile allomones as kairomones. These facts speak for an adaptation of insects to plant physiology and a limited importance of phytophagous insects in selection pressure upon plants. Herbivorous insects have realized specific adaptations to be able to discriminate between complex odour blends, but the utilization of chemical groups among insect taxa is different.The main theories on plant chemical defence do not discuss the impact of volatiles on host plant selection and may be apt to revision when pheromones, allomones, kairomones and synomones are not taken into account.     

Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians

While often studied in isolation, host-parasite interactions are typically embedded within complex communities. Other community members, including predators and alternative hosts, can therefore alter parasite transmission (e.g., the dilution effect), yet few studies have experimentally evaluated more than one such mechanism. Here, we used data from natural wetlands to design experiments investigating how alternative hosts and predators of parasites mediate trematode (Ribeiroia ondatrae) infection in a focal amphibian host (Pseudacris regilla). In short-term predation bioassays involving mollusks, zooplankton, fish, larval insects, or newts, four of seven tested species removed 62-93% of infectious stages. In transmission experiments, damselfly nymphs (predators) and newt larvae (alternative hosts) reduced infection in P. regilla tadpoles by -50%, whereas mosquitofish (potential predators and alternative hosts) did not significantly influence transmission. Additional bioassays indicated that predators consumed parasites even in the presence of alternative prey. In natural wetlands, newts had similar infection intensities as P. regilla, suggesting that they commonly function as alternative hosts despite their unpalatability to downstream hosts, whereas mosquitofish had substantially lower infection intensities and are unlikely to function as hosts. These results underscore the importance of studying host-parasite interactions in complex communities and of broadly linking research on predation, biodiversity loss, and infectious diseases.     

Effects of predator visibility on prey encounter: a case study on aerial web weaving spiders

Summary Perhaps the most important factor affecting predator-prey interactions is their encounter probability. Predators must either locate sites where prey are active or attract prey to them, and prey must be able to recognize potential predators and flee before capture. In this study we manipulate and describe three components of the foraging system of predatory, web-weaving spiders, the presence of viscid droplets, silk brightness (achromatic surface reflectance), and visibility of the orb pattern, to determine their effect on insect attraction, recognition, and web avoidance. We found that webs with viscid droplets were more visible to prey at close range, but at greater distances the sparkling droplets lured insects to the web area and hence increased insect capture probability. Although the size of viscid droplets and silk brightness are closely correlated (Table 2, Fig. 3), the relationships among droplet size, spider size, and the visual environments in which webs are found are more complicated (Fig. 2, Tables 2, 3). In environments with predictable light exposure, droplet size and hence silk visibility correlate with spider size, and spiders that forage at night produce relatively more visible silks then spiders that forage during the day (Table 3, Fig. 4). In habitats in which light levels are not predictable, silk surface reflectance and spider size are not closely correlated, suggesting that the complexity of the light environment, as well as the visual and foraging behaviors of insects found there, has played an important role in the evolution of spider-insect interactions.Offprint requests to: C.L. Craig     

Production of semiochemical and allelobiotic agents as a consequence of aphid feeding

Aphids have an extremely intimate relationship with their plant hosts. Although this might suggest that aphid infestation would be largely cryptic, there are a wide range of changes that can be detected behaviourally, chemically and also at the molecular genetic level. Colonisation by aphids can cause release of semiochemicals characteristic of the aphid species and besides reducing acceptability to incoming aphids; these can enable recruitment of specific parasitoids. Some semiochemicals involved in these processes can also influence the defence status of neighbouring intact plants through air or the rhizosphere. Electrophysiological and behavioural studies on the aphids, their parasitoids and other organisms facilitate the identification of compounds having direct effects on plant defence. New developments from work on semiochemicals such as (Z)-jasmone and 6-methyl-5-hepten-2-one, and allelobiotic agents such as 6-hydroxy-1,2,3,4-tetrahydro-β-carboline-3-carboxylic acid and 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one, as well as new work on these compounds and others as potential phytopheromones are discussed.     

Trapping pheromonal components with silicone rubber tubes: fatty acid secretions in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Summary. We describe the use of pieces of silicone tubing to analyse the mandibular gland components of queen and worker honeybees and show that these compounds can be efficiently trapped on bis(trimethylsilyl)trifluoroacetamide (BSTFA) treated pieces of tubing. The use of this technique rather than that of solid phase microextraction (SPME) techniques with commercially available fibres that have been shown to be efficient at sampling secretions from the cuticle of insects, is necessitated by a requirement for collection of large sample numbers in a short space of time or for sampling in the field. The technique may be generalised for use with semiochemicals of low volatility in other insect communciation systems.     

Mother really knows best: host choice of adult phytophagous insect females reflects a within-host variation in suitability as larval food

Non-random distribution patterns of specialized phytophagous insects on their hosts may depend on intraspecific differences in plant tissue quality, including nutrients and secondary compounds. Secondary compounds are involved in plant resistance, but are also important for the recognition and acceptability of plants as resources by specialized insects. If individuals within a plant species vary in their content of such secondary substances, there may also be qualitative differences between them. In such cases, natural selection will favor insects with the ability to distinguish and prefer the more suitable plants. In Sweden, the leaf beetle Gonioctena linnaeana Schrank (Coleoptera, Chrysomelidae) is highly specialized on one host, the native willow Salix triandra L (Salicaceae). Field observations reveal that some host plants in a population harbor many feeding larvae, causing severe defoliation, whereas neighboring plants may have few or no feeding larvae. Our hypothesis is that the distribution pattern of G. linnaeana larvae in this population results from qualitative differences between individual host plants in combination with the ability of G. linnaeana females to distinguish between plants that are suitable and not suitable for offspring performance. We examine whether larval survival differs depending on diet and whether the content of secondary chemical compounds explains female preference. Based on the higher survival rate of larvae reared on leaves from preferred hosts, we conclude that G. linnaeana females have evolved a behavior that maximizes offspring performance and thus positively affects female fitness. A chemical survey of the plants indicates that luteolin-7-glucoside and an unidentified flavonoid are important for separating the preferred from the non-preferred plants.     

Modern Insect Extinctions, the Neglected Majority

Abstract:  Most extinctions estimated to have occurred in the historical past, or predicted to occur in the future, are of insects. Despite this, the study of insect extinctions has been neglected. Only 70 modern insect extinctions have been documented, although thousands are estimated to have occurred. By focusing on some of the 70 documented extinctions as case studies, I considered ways in which insect extinctions may differ from those of other taxa. These case studies suggested that two types of extinction might be common for insects but rare for other taxa: extinction of narrow habitat specialists and coextinctions of affiliates with the extinctions of their hosts. Importantly, both of these forms of extinction are often ignored by conservation programs focused on vertebrates and plants. Anecdotal evidence and recent simulations suggest that many insect extinctions may have already occurred because of loss of narrow habitat specialists from restricted habitats and the loss of hosts. If we are serious about insect conservation, we need to spend more time and money documenting such extinctions. To neglect such extinctions is to ignore the majority of species that are or were in need of conservation.     

Plant chemistry and insect sequestration

Most plant families are distinguished by characteristic secondary metabolites, which can function as putative defence against herbivores. However, many herbivorous insects of different orders can make use of these plant-synthesised compounds by ingesting and storing them in their body tissue or integument. Such sequestration of putatively unpalatable or toxic metabolites can enhance the insects’ own defence against enemies and may also be involved in reproductive behaviour. This review gives a comprehensive overview of all groups of secondary plant metabolites for which sequestration by insect herbivores belonging to different orders has been demonstrated. Sequestered compounds include various aromatic compounds, nitrogen-containing metabolites such as alkaloids, cyanogenic glycosides, glucosinolates and other sulphur-containing metabolites, and isoprenoids such as cardiac glycosides, cucurbitacins, iridoid glycosides and others. Sequestration of plant compounds has been investigated most in insects feeding or gathering on Apocynaceae s.l. (Apocynoideae, Asclepiaoideae), Aristolochiaceae, Asteraceae, Boraginaceae, Fabaceae and Plantaginaceae, but it also occurs for some gymnosperms and even lichens. In total, more than 250 insect species have been shown to sequester plant metabolites from at least 40 plant families. Sequestration predominates in the Coleoptera and Lepidoptera, but also occurs frequently in the orders Heteroptera, Hymenoptera, Orthoptera and Sternorrhyncha. Patterns of sequestration mechanisms for various compound classes and common or individual features occurring in different insect orders are highlighted. More research is needed to elucidate the specific transport mechanisms and the physiological processes of sequestration in various insect species.     

Echolocation call design and limits on prey size: a case study using the aerial-hawking bat Nyctalus leisleri

The echolocation calls used by Nyctalus leisleri during search phase in open air space are between 9 and 14 ms long, with the peak energy between 24 and 28 kHz. The pulses are shallowly frequency-modulated with or without an initial steep frequency-modulated component. The diet consists primarily of small flies (Diptera), including many chironomids (wingspan 9–12 mm) and yellow dung flies (Scatophaga; wingspan 24 mm), but also of some larger insects such as dung beetles (Coleoptera; Scarabaeoidea), caddis-flies (Trichoptera) and moths (Lepidoptera). The echo target strength of some prey items was measured. Contrary to models based on standard targets such as spheres or disks, the echo strength of real insects was found to be virtually independent of the emitted frequency within the 20–100 kHz frequency range. A model was used to calculate probable detection distances of the prey by the bat. Using narrow-band calls of 13.7 ± 2.7 ms duration, a bat would detect the two smallest size classes of insect at greatest range using calls of 20 kHz. The results may therefore explain why many species of large and medium sized aerial-hawking bats use low-frequency calls and still eat mostly relatively small insects. The data and model challenges the assumption that small prey are unavailable to bats using low-frequency calls.     

Adaptation of a four-arm olfactometer for behavioural bioassays of large beetles

Summary. We adapted a four-arm olfactometer (55 × 55 × 5.5 cm) for bioassays of large insects and its usefulness was evaluated by testing the responses of three beetles, the palm weevil Rhynchophorus palmarum (L.) (Coleoptera: Curculionidea) and two Dynast scarabs Strategus aloeus (L.) and Oryctes rhinoceros (L.) (Coleoptera: Scarabaeidae) to plant odours and aggregation pheromones. This olfactometer was coupled to a volatile delivery system dispensing highly volatile semiochemicals at constant concentrations. We materialized airflows in the olfactometer by discolouring sensitive papers with acid vapours under various conditions (air straighten by stainless steel grids in inputs and output, 500 ml/min per arm) to visualize air turbulence and to test air-tightness. The volatile delivery system can be used to mix and dispense a broad range of concentrations of semiochemicals in air from diluted aqueous solutions. It was calibrated by measuring the release of the pheromone using solid phase-microextraction (SPME). Dose-response curves to synthetic pheromone were obtained for O. rhinoceros of both sexes. Coupling the volatile delivery system to the fourarm olfactometer provided a system with which the responses of R. palmarum and S. aloeus to their synthetic aggregation pheromones and to natural plant volatiles could be readily observed and studied.     

Multiple techniques confirm elevational differences in insect size that may influence spider sociality

Social and subsocial spiders of the genus Anelosimus exhibit an altitudinal pattern in their geographic distribution at tropical latitudes in the Americas. Social species, which capture prey cooperatively, occur primarily in the lowland rain forest and are absent from higher elevations, whereas subsocial species are common at higher elevations but absent from the lowland rain forest. Previous studies have suggested that differences in the size of potential insect prey along altitudinal gradients may explain this pattern as insects were found to be, on average, larger in lowland rain forests than at higher elevations. These studies, however, may have under-sampled the insect size composition of each habitat because only one sampling technique was used. Using a number of collection methods we sampled the insect size composition in the environments of social and subsocial spiders in this genus. We found that the average insect size in lowland rain forest habitats was indeed larger than at high-elevation cloud forests in eastern Ecuador. We also found that, even though the various techniques differed in the size of the insects they captured (visual searching and blacklighting yielding larger insects than beating, sweeping, or malaise trapping), they all caught, on average, larger insects in the lowlands. Overall, spider colonies in the lowlands caught larger prey than did spider colonies at higher elevations, paralleling differences in insect size distribution obtained by the various techniques in their respective environments.     

The use of Doppler-shifted echoes as a flutter detection and clutter rejection system: the echolocation and feeding behavior of Hipposideros ruber (Chiroptera: Hipposideridae)

Summary Hipposideros ruber use CF/FM echolocation calls to detect the wing flutter of their insect prey. Fluttering prey were detected whether the insects were flying or sitting on a surface, and prey in either situation were captured with equal success (approximately 40% of capture attempts). Stationary prey were ignored. The bats did not use visual cues or the sounds of wing flutter to locate their prey. Wing flutter detection suggests that H. ruber exploit the Doppler-shifted information in echoes of their echolocation calls. These bats fed primarily upon moths, usually those of between 10 and 25 mm wingchord, although moths of less than 5 mm and greater than 40 mm wingchord were also attacked and captured. They showed no evidence of selecting moths on the basis of species or other taxonomic distinction, and occasionaly captured other insects.     

Brazilian free-tailed bats as insect pest regulators in transgenic and conventional cotton crops.

During the past 12000 years agricultural systems have transitioned from natural habitats to conventional agricultural regions and recently to large areas of genetically engineered (GE) croplands. This GE revolution occurred for cotton in a span of slightly more than a decade during which a switch occurred in major cotton production areas from growing 100% conventional cotton to an environment in which 95% transgenics are grown. Ecological interactions between GE targeted insects and other insectivorous insects have been investigated. However, the relationships between ecological functions (such as herbivory and ecosystem transport) and agronomic benefits of avian or mammalian insectivores in the transgenic environment generally remain unclear, although the importance of some agricultural pest management services provided by insectivorous species such as the Brazilian free-tailed bat, Tadarida brasiliensis, have been recognized. We developed a dynamic model to predict regional-scale ecological functions in agricultural food webs by using the indicators of insect pest herbivory measured by cotton boll damage and insect emigration from cotton. In the south-central Texas Winter Garden agricultural region we find that the process of insectivory by bats has a considerable impact on both the ecology and valuation of harvest in Bacillus thuringiensis (Bt) transgenic and nontransgenic cotton crops. Predation on agricultural pests by insectivorous bats may enhance the economic value of agricultural systems by reducing the frequency of required spraying and delaying the ultimate need for new pesticides. In the Winter Garden region, the presence of large numbers of insectivorous bats yields a regional summer dispersion of adult pest insects from Bt cotton that is considerably reduced from the moth emigration when bats are absent in either transgenic or non-transgenic crops. This regional decrease of pest numbers impacts insect herbivory on a transcontinental scale. With a few exceptions, we find that the agronomics of both Bt and conventional cotton production is more profitable when large numbers of insectivorous bats are present.     

Protection from Natural Enemies in Managing Rare Plant Species

Abstract: Natural enemies such as pathogens, herbivores, and seed predators can substantially limit the abundance of plants, including rare species. Vulnerability to particular enemies is likely to differ between life-history stages. We hypothesized that short-term protection of juvenile plants from herbivores can be used to increase population growth of rare species and thus improve the probability of long-term persistence. Using the federally listed (threatened) Pitcher's thistle ( Cirsium pitcheri ) as a model, we experimentally excluded insect herbivores from juvenile rosettes to evaluate the potential benefits of deliberate insect control as a tool for management of rare species. Herbivore effects varied spatially across the local environment. Excluding insects in portions of the habitat where herbivory was high had direct benefits, including a 53% decrease in juvenile plant mortality (60% to 7%) and a 10-fold increase in seed production of juveniles that matured and flowered. In other areas, where herbivore-induced juvenile mortality was relatively low, excluding insects either increased seed production of plants that flowered or had no major effect. Our data also suggest indirect benefits to the metapopulation via potential improvement in dispersal among patches. Temporal variation in growing conditions occurred between years, suggesting that multiple-year exclusions would be most effective. Our study suggests that small–scale manipulation of often inconspicuous interactions between rare plants and their natural enemies can be an effective, relatively low-cost tool for the management and restoration of rare plant species.     

Social spiders catch larger prey: a study of Anelosimus eximius (Araneae: Theridiidae)

Summary During a 1-year-study in tropical Panama, prey of the social theridiid Anelosimus eximius was analysed at two locations and compared with the potential prey spectrum according to sweepnet catches, pitfall traps and bowl traps. Compared with other web-building spiders, A. eximius catch an unusually high number of large insects: about 90% are flying ants, beetles,lepidopterans hemipterans, cockroaches and grasshoppers. This is the result of a communal strategy to overwhelm prey. Webs are maintained commonly, and several spiders attack an entangled insect simultaneously. More spiders participate on insects that are larger and struggle more. The ability to catch large prey insects is discussed as a major driving factor for sociality in spiders.     

Impact of an invasive oak gall wasp on a native butterfly: a test of plant-mediated competition

Phytophagous insects commonly interact through shared host plants. These interactions, however, do not occur in accordance with traditional paradigms of competition, and competition in phytophagous insects is still being defined. It remains unclear, for example, if particular guilds of insects are superior competitors or important players in structuring insect communities. Gall-forming insects are likely candidates for such superior competitors because of their ability to manipulate host plants, but their role as competitors is understudied. We investigate the effect of invasive populations of an oak gall wasp, Neuroterus saltatorius, on a native specialist butterfly, Erynnis propertius, as mediated by their shared host plant, Quercus garryana. This gall wasp occurs at high densities in its introduced range, where we stocked enclosures with caterpillars on trees that varied in gall wasp density. Biomass production of butterflies was lower in enclosures on high-density than on low-density trees because overwintering caterpillars were smaller, and fewer of them eclosed into adults the following spring. To see if the gall wasp induced changes in foliar quality, we measured host plant quality before and after gall induction on 30 trees each at two sites. We found a positive relationship between gall wasp density and the percentage change in foliar C:N, a negative relationship between gall wasp density and the percentage change in foliar water at one site, and no relationship between the percentage change in protein-binding capacity (i.e., phenolics) and gall-wasp density. Additionally, there was a negative relationship between foliar quality and butterfly performance. Our results provide evidence for a plant-mediated impact of an invasive oak gall wasp on a native butterfly and suggest that gall wasps could act as superior competitors, especially when they occur at high densities.     

Effects of Elevated Atmospheric Carbon Dioxide on Insect-Plant Interactions

Abstract: In the enriched carbon dioxide atmosphere expected in the next century, many species of herbivorous insects will confront less nutritious host plants that will induce both lengthened larval developmental times and greater mortality. The limited data currently available suggest that the effect of increased atmospheric CO₂ on herbivory will be not only highly species-specific but also specific to each insect-plant system. Several scenarios can be predicted, however: (1) local extinctions will occur; (2) the endangered species status as well as the pest status of some insect species will change; (3) geographic distributions for some insect species will shift with host-plant ranges; and (4) changes in the population dynamics of affected insect species will influence their interactions with other insects and plants. For insect conservation purposes, it is critical to begin long-term studies on the effects of enhanced CO₂ levels on insect populations. An analysis of the available literature indicates that many orders containing insect species important for ecosystem conservation, and even those important as agricultural or medical pests, have not been examined. Without a major increase in research on this topic, we will be unprepared for the species changes that will occur, we will lose the opportunity to document just how some insects adapt to elevated CO₂ levels, and we will lack the information necessary for effective conservation efforts.     

Herbivore species, infestation time, and herbivore density affect induced volatiles in tea plants

In response to insect herbivory, plants emit volatiles that are used by the herbivores’ natural enemies to locate their host or prey. Herbivore attack also enhances tea aroma. Herbivore-induced plant volatiles (HIPVs) vary both quantitatively and qualitatively with infestation duration and herbivore density. Thus, whether HIPVs can reliably communicate the identities of herbivores is of interest. Here, we studied the tea plant volatiles induced by the tea leafhopper (Empoasca vitis, a piercing–sucking insect), the tea geometrid (Ectropis oblique, a chewing insect), and methyl jasmonate (MeJA, a plant hormone). Geometrid feeding induced more complex volatile blends than did leafhopper infestation. The volatiles induced by both herbivores significantly increased in quality and quantity with time during the first 16 h of infestation, after which the profiles of induced volatile blends and the emission of induced compounds varied diurnally. (E)-β-Ocimene displayed a unique rhythm in which emission peaked at night. The amount of HIPVs significantly increased, while their profiles changed little, with herbivore density. Overall, the leafhoppers and geometrids induced significantly different volatiles from tea plants, while the HIPV profiles varied with a circadian rhythm and were similar at different herbivore densities. Our findings also suggest a new method of enhancing tea flavor using exogenously applied plant hormones, because the volatiles induced by leafhoppers and MeJA were similar in general composition.     

Why are warning displays multimodal?

Multimodal defensive displays are commonplace, with prey combining conspicuous coloration, sounds, odours and other chemical emissions to deter predators. These components can signal to predators in multiple signal modalities to warn them that prey are defended. The aim of our review is to examine the form and function of multimodal warning displays. Data collected from the literature on multimodal insect warning displays show the degree of complexity and diversity that needs to be explained, and we identify patterns in the data that may be worthy of more rigorous investigation. We also provide a theoretical framework for the study of multimodal warning displays, and evaluate the evidence for different functional hypotheses that can explain their widespread evolution. Our review highlights that whilst multimodal warning displays are well documented, particularly in insects, we lack a good understanding of their function in natural predator–prey systems.     

Intraguild predation by <Emphasis Type="Italic">Harmonia axyridis</Emphasis> on coccinellids revealed by exogenous alkaloid sequestration

Summary.  Under laboratory conditions, the multicolored Asian lady beetle, Harmonia axyridis is well known as an intraguild predator of other ladybirds. However the real impact of this exotic species on native species was poorly investigated in the field. Because many ladybird species produce alkaloids as defensive compounds, we propose here a new method of intraguild predation monitoring in coccinellids based on alkaloid quantification by GC-MS. In laboratory experiments, adaline was unambiguously detected in fourth instar larvae of H. axyridis having ingested one egg or one first instar larva of Adalia bipunctata. Although prey alkaloids in the predator decreased with time, traces were still detected in pupae, exuviae and imagines of H. axyridis having ingested one prey when they were fourth instar larvae. Analysis of H. axyridis larvae collected in two potato fields shows for the first time in Europe the presence of exogenous alkaloids in 9 out of 28 individuals tested. This new method of intraguild predation detection could be used more widely to follow the interactions between predators and potential chemically defended insect preys.