H. Dijkman

Herbivory induces systemic production of plant volatiles that attract predators of the herbivore : extraction of endogenous elicitor

It was previously shown that in response to infestation by spider mites (Tetranychus urticae), lima bean plants produce a volatile herbivoreinduced synomone that attracts phytoseiid mites (Phytoseiulus persimilis) that are predators of the spider mites. The production of predator-attracting infochemicals was established to occur systemically throughout the spider mitein-fested plant. Here we describe the extraction of a water-soluble endogenous elicitor from spider mite-infested lima bean leaves. This elicitor was shown to be transported out of infested leaves and was collected in water in which the petiole of the infested leaf was placed. When the petioles of uninfested lima bean leaves were placed in water in which infested leaves had been present for the previous seven days, these uninfested lima bean leaves became highly attractive to predatory mites in an olfactometer when an appropriate control of uninfested lima bean leaves was offered as alternative. The strength of this effect was dependent on the number of spider mites infesting the elicitor-producing leaves. Higher numbers of spider mites resulted in an elicitor solution with a stronger effect. In addition, spider mite density was important. The elicitor obtained from one leaf with 50 spider mites had a stronger effect on the attractiveness of uninfested leaves than the elicitor obtained from three leaves with 17 spider mites each. This suggests that the stress intensity imposed on a plant is an important determinant of the elicitor quantity. While the elicitor has a strong effect on the attractiveness of uninfested leaves, spider mite-infested leaves are still much more attractive to predatory mites than elicitor-exposed leaves. The data are discussed in the context of systemic effects in plant defense and the biosynthesis of herbivore-induced terpenoids in plants.

INDUCTION OF DIRECT AND INDIRECT PLANT RESPONSES BY JASMONIC ACID, LOW SPIDER MITE DENSITIES, OR A COMBINATION OF JASMONIC ACID TREATMENT AND SPIDER MITE INFESTATION

Jasmonic acid (JA) and the octadecanoid pathway are involved in both induced direct and induced indirect plant responses. In this study, the herbivorous mite, Tetranychus urticae, and its predator, Phytoseiulus persimilis, were given a choice between Lima bean plants induced by JA or spider mites and uninduced control plants. Infestation densities resulting in the induction of predator attractants were much lower than thus far assumed, i.e., predatory mites were significantly attracted to plants that were infested for 2 days with only one or four spider mites per plant. Phytoseiulus persimilis showed a density-dependent response to volatiles from plants that were infested with different numbers of spider mites. Similarly, treating plants with increasing concentrations of JA also led to increased attraction of P. persimilis. Moreover, the duration of spider mite infestation was positively correlated with the proportion of predators that were attracted to mite-infested plants. A pretreatment of the plants with JA followed by a spider mite infestation enhanced the attraction of P. persimilis to plant volatiles compared to attraction to volatiles from plants that were only infested with spider mites and did not receive a pretreatment with JA. The herbivore, T. urticae preferred leaf tissue that previously had been infested with conspecifics to uninfested leaf tissue. In the case of choice tests with JA-induced and control leaf tissue, spider mites slightly preferred control leaf tissue. When spider mites were given a choice between leaf discs induced by JA and leaf discs damaged by spider mite feeding, they preferred the latter. The presence of herbivore induced chemicals and/or spider mite products enhanced settlement of the mites, whereas treatment with JA seemed to impede settlement.

Within-plant circulation of systemic elicitor of induced defence and release from roots of elicitor that affects neighbouring plants

Herbivory on the above-ground plant parts can induce the production of volatiles that attract carnivorous enemies of the herbivores. These volatiles may be induced systemically in the damaged plant. In a previous study, we had shown that a systemic elicitor that induces the production of predator-attracting volatiles in lima bean plants can be collected from lima bean leaves by placing spider-mite-infested leaves with their petiole in water. However, it remained unknown to what sites this elicitor was transported within the plant. Here, we show that exposing uninfested lima bean leaves to this elicitor also results in a reduced rate of reproduction in spider mites (Tetranychus urticae). Furthermore, an elicitor can also be collected from whole lima bean plants of which one primary leaf was infested with spider mites, by detaching the other primary leaf and inserting the petiole, that is still connected to the plant, in a vial with distilled water. When uninfested lima bean leaves are incubated in this elicitor solution for three days, this results in the attraction of the predatory mite Phytoseiulus persimilis in an olfactometer. Finally, an elicitor of predator-attracting volatiles was collected from whole infested lima bean plants by placing the plants with their roots in distilled water. Uninfested lima bean plants that were subsequently placed with their roots in this water became attractive to the predatory mite P. persimilis relative to control plants that had been placed with their roots in water in which uninfested bean plants had been incubated previously. These data indicate that herbivore-infested plants may interact with undamaged neighbouring plants through chemical information that is exchanged in the soil. Important issues that need to be addressed next are discussed. The connection of above- and below-ground interactions of plants with other organisms will have important consequences for future ecological studies on multitrophic interactions.

Nitrogen Availability and Defense of Tomato Against Two-spotted Spider Mite

The aim of this work was to study how nitrogen availability affects within-plant allocation to growth and secondary metabolites and how this allocation affects host selection by herbivores. Tomato plants (Lycopersicon esculentum) were grown at six levels of nitrogen availability. When nitrogen availability increased, plant relative growth rate increased, but tissue carbon/nitrogen ratio in the second oldest true leaf and allocation to large glandular trichomes (type VI) as well as to the defense compounds rutin and chlorogenic acid decreased. Leaf protein concentration increased. Two-spotted spider mite (Tetranychus urticae) females responded significantly to these changes: in dual choice tests they preferred leaf disks from plants grown at high nitrogen availability, with a low C/N ratio. This preference persisted in an olfactometer in which the mites were offered only the odors released by leaves with damaged trichomes. We conclude that in a tomato leaf increased nitrogen availability leads to decreased allocation to defenses, and that repellent volatiles released by trichomes play a key role in affecting leaf selection by two-spotted spider mite females.

Induced defence in detached uninfested plant leaves: effects on behaviour of herbivores and their predators

SummaryInduction of plant defence against herbivores may include the attraction by volatile infochemicals of natural enemies of the herbivore. The emitted volatiles that mediate this attraction may also affect the behaviour of the herbivore itself. In this paper we investigate the response of the herbivorous spider miteTetranychus urticae and the predatory mitePhytoseiulus persimilis towards volatiles whose production is induced in detached Lima bean leaves. Detached uninfested Lima bean leaves were incubated on wet cotton wool on which bean leaves infested with spider mites (T. urticae) were present simultaneously or had been present previously. These treatments induce the production of volatile infochemicals in the uninfested bean leaf tissue: predatory mites are attracted and spider mites are deterred. These are the first data on the response of predators and herbivores to plant volatiles whose production was induced in detached uninfested leaves.

Change in foraging behaviour of the predatory mite Phytoseiulus persimilis after exposure to dead conspecifics and their products

Adult females of the predatory mite Phytoseiulus persimilis Athias‐Henriot are strongly attracted to infochemicals released by plants infested with their prey, the two‐spotted spider mite (Tetranychus urticae Koch), thereby effectively locating their prey. However, we found a consistently lower degree of attraction to these infochemicals for a population of P. persimilis, which is called non‐responding population. Here we demonstrate that this low degree of attraction is a contagious phenomenon and that it cannot be explained by differences in abiotic conditions, physiological state and experience of predators or by genetic differences between predator populations. Female predators exposed to dead conspecifics of the non‐responding population and their products showed a lower degree of attraction to plant odours and a higher mortality than predators exposed to products of a living conspecific of the non‐responding population. This was true 6–7 days after contact with dead conspecifics and their products whereas 2 days after contact no effects were detected. The present results are discussed in view of our hypothesis that the change in foraging behaviour as well as the high mortality rate are symptoms of a contagious disease affecting the non‐responding population.

Change in Behavioral Response to Herbivore-induced Plant Volatiles in a Predatory Mite Population

Damage by herbivorous spider mites induces plants to produce volatiles that attract predatory mites that consume the spider mites. A clear attraction to volatiles from Lima bean plants infested with the spider mite Tetranychus urticae has been consistently reported during more than 15 years for the predatory mite Phytoseiulus persimilis. We have monitored the response to volatiles from spider-mite infested Lima bean plants for a laboratory population of the predatory mite from 1991 to 1995 on a regular basis. A reduction in the level of attraction in the laboratory population of P. persimilis was recorded in mid-1992. The attraction of the laboratory population was weaker than that of a commercial population in the latter part of 1992, but the responses of these two populations were similarly weak in 1994 and 1995. Therefore, a behavioral change has also occurred in this commercial population. Experiments were carried out to address the potential causes of this change in attraction. The attraction of predators from a commercial population with a strong response decreased after being reared in our laboratory. Within a predator population with a low degree of attraction, strongly responding predators were present and they could be isolated on the basis of their behavior: predators that stayed on spider-mite infested plants in the rearing set-up had a strong attraction, while predators that had dispersed from the rearing set-up were not attracted to prey-infested bean plants. From our laboratory population with a low degree of attraction, isofemale lines were initiated and maintained for more than 20 generations. All isofemale lines exhibited a consistently strong attraction to spider mite-induced plant volatiles, similar to the attraction recorded for several populations in the past 15 years. Neither in a population with a strong attraction nor in two with a weak attraction was the response of the predators affected by a starvation period of 1–3 hr. Based on these results, possible causes for the observed reduction in predator attraction to spider mite-induced bean volatiles are discussed. The predatory mite P. persimilis is a cornerstone of biological control in many crops worldwide. Therefore, the change in foraging behavior recorded in this predator may have serious consequences for biological control of spider mites.