Bas Drukker

Volatiles from Psylla-infested pear trees and their possible involvement in attraction of anthocorid predators

Previous work showed that anthocorid predators aggregate around gauze cages containing Psylla-infested trees in a pear orchard. Because anthocorids responded to odor from Psylla-infested leaves in a laboratory test, it was hypothesized that these aggregative responses in the field were triggered by olfaction of compounds associated with Psylla injury. We present chemical analyses of volatiles from damaged and undamaged plants and studies on behavioral responses of anthocorid predators to compounds released by damaged plants. Leaf headspace volatiles from clean and Psylla-infested pear trees were collected on Tenax and identified by GC-MS after thermodesorption. Twelve volatiles were found exclusively in headspace samples from Psylla-infested leaves. Six were present in significantly higher quantities in samples from infested leaves: the monoterpene, (E,E)-α-farnesene, the phenolic, methyl salicylate, and the green leaf compounds, (Z)-3-hexen-1-yl acetate, (Z)-3-hexen-1-ol, 1-hexyl-acetate, and 1-penten-3-ol. These compounds are known to be produced by plants, and damage by pear psyllids seems to trigger their emission. Blend composition varied and was partly correlated with tree or leaf age and degree of Psylla infestation. To study whether compounds associated with leaf injury elicit olfactory responses in anthocorid predators, apple-extracted (E,E)-α-farnesene, synthetic methyl salicylate, and (Z)-3-hexen-1-yl acetate were offered in a Y-tube olfactometer to field-collected adult Anthocoris spp. Significant positive responses were found to both the monoterpene and the phenolic, but not to the green leaf volatile. The results lend support to the hypothesis that predator attraction to herbivore-infested pear trees is mediated by herbivory-induced plant volatiles.

Do anthocorid predators respond to synomones from Psylla-infested pear trees under field conditions?

Because Y‐tube olfactometer experiments in the laboratory showed a response of anthocorid bugs to odour from Psylla‐infested leaves, it was of interest to assess its relevance under field circumstances. This was done by measuring the density of predatory bugs on pear trees adjacent to Psylla‐infested or control trees that were covered with fine mesh gauze‐screens. In this way odours from these caged trees could spread through the screen, while contact with the Psylla prey in the cage was prevented. The density of anthocorid predators around cages with heavily infested trees was significantly higher than around uncaged control trees and around cages containing uninfested or little infested trees. Covering a cage with Psylla‐infested trees by an airtight plastic sheet led to an immediate drop in the density of anthocorid predators, whereas removal of the sheet led to predator aggregation again. The results of these field experiments strongly support the hypothesis that anthocorid predators respond to volatile chemicals emanating from Psylla‐infested pear trees.

Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey.

We investigated how the plant‐inhabiting, anthocorid predator, Anthocoris nemoralis, copes with variation in prey, host plant and associated herbivore‐induced plant volatiles and in particular whether the preference for these plant odours is innate or acquired. We found a marked difference between the olfactory response of orchard‐caught predators and that of their first generation reared on flour moth eggs in the laboratory, i.e. under conditions free of herbivory‐induced volatiles. Whereas the orchard‐caught predators preferred odour from psyllid‐infested pear leaves, when offered against clean air in a Y‐tube olfactometer, the laboratory‐reared first generation of (naive) predators did not. The same difference was found when a single component (methyl salicylate) of the herbivore‐induced plant volatiles was offered against clean air. After experiencing methyl salicylate with prey, however, the laboratory‐reared predators showed a pronounced preference for this volatile. This acquired preference did not depend on whether the volatile had been experienced in the juvenile period or in the adult phase, but it did depend on whether it had been offered in presence or absence of prey. In the first case, they were attracted to the plant volatile in subsequent olfactometer experiments, but when the volatile had been offered during a period of prey deprivation, the predators were not attracted. We conclude that associative learning is the most likely mechanism underlying acquired odour preference.

How Predatory Mites Learn to Cope with Variability in Volatile Plant Signals in the Environment of their Herbivorous Prey

When the chemical cues co-occurring with prey vary in time and space, foraging predators profit from an ability to repeatedly associate chemical cues with the presence of their prey. We demonstrate the ability of a predatory arthropod (the plant-inhabiting mite, Phytoseiulus persimilis) to learn the association of a positive stimulus (herbivorous prey, Tetranychus urticae) or a negative stimulus (hunger) with a chemical cue (herbivore-induced plant volatiles or green leaf volatiles). It has been suggested that the rate at which the integration of information becomes manifest as a change in behaviour, differs between categories of natural enemies (parasitoids versus insect predators; specialist versus generalist predators). We argue that these differences do not necessarily reflect differential learning ability, but rather relate to the ecologically relevant time scale at which the biotic environment changes.

Constitutive and herbivore-induced volatiles in pear, alder and hawthorn trees

Summary. Qualitative and quantitative differences among pear cultivars were found in constitutive and Cacopsylla-induced volatiles, depending on experimental treatment of the trees (i.e., uninfested and partly or completely infested by psyllids). Blend differences were also found between pear cultivars and wild-type pear, alder and hawthorn–the latter trees are frequently present in pear orchard hedgerows. ¶Interesting differences were found in the presence of methyl salicylate and (E,E)-α-farnesene, two compounds previously found to mediate attraction of predatory bugs towards psyllid-infested pear trees. Methyl salicylate is expressed constitutively and is induced systemically by infestation in the whole plant of all four cultivars. (E,E)-α-farnesene on the other hand showed also systemic induction in Bartlett, NY10355 and Beurré Hardy, but in partially infested Conference trees it was induced locally, only in herbivore-damaged leaves. No methyl salicylate or (E,E)-α-farnesene were identified in honeydew. In field collected headspace samples of alder leaves infested by aphids and leaf beetles we found methyl salicylate but no (E,E)-α-farnesene, whereas in uninfested hawthorn neither were identified. Insight in the variability of damage-related pear volatiles will have important implications for integrated pest management in the field.

Improved control capacity of the mite predator Phytoseiulus persimilis (Acari: Phytoseiidae) on tomato

The predatory mite Phytoseiulus persimilis is frequently reported to perform poorly on greenhouse tomatoes. As the predators are mass-reared on another host plant (bean), we supposed that they are poorly adapted to tomato, a plant densely packed with poisonous and sticky glandular hairs. This hypothesis was tested by comparing the control capacity of a stain of P. persimilis directly obtained from a mass rearing with the same strain after four generations on tomato. Both strains were released in a tomato crop in two identical compartments of a greenhouse and the population dynamics of prey (a tomato strain of Tetranychus urticae) and predator were recorded at weekly time intervals. It was found that the strain previously exposed to a tomato environment performed better than the unexposed strain: (1) its population increased faster; (2) the prey population declined faster; and (3) the damage to new-grown tomato leaves was considerably lower. To investigate the causes of the difference in performance between the exposed and unexposed strains, oviposition and survival rates were assessed on a diet of two-spotted spider mites on tomato leaf sections. In addition, the unexposed strain was tested on a diet of two-spotted spider mites on bean leaf sections. The difference in oviposition rates of both predator strains was small compare to the overall mean. However, the oviposition rate of the first generation of predators since transfer from bean to tomato dropped to less than half of the original value. Moreover, mortality in the first generation increased from 14% to 89%, whereas it decreased to 0% after four generations. Future research should clarify whether these changes in life history are due to selection or to physiological adaptation.

Interactions between arthropod predators and plants: A conspiracy against herbivorous arthropods?

Plants provide protection (domatia), alternative food (nectar, exudates, pollen) and chemical lures which benefit predatory arthropods and thereby protect plants against herbivorous arthropods. Experimental evidence for these indirect effects is reviewed and hypotheses are provided to explain why plants invest in attracting, feeding and protecting predatory arthropods despite the fact that (1) other organisms not beneficial to the plant may utilize these facilities too, and (2) also competing neighbour-plants may profit from these investments. It is argued that although the plant may benefit under certain conditions, plant-bodyguard interactions do not have a single anticipated outcome. Instead, these interactions may have a range of positive, neutral and negative outcomes, the exact value of which depends on position in space and moment in time. The benefits to the plant investing in indirect defence depend on the availability and responsiveness of predatory arthropods, the abundance and responses of cheaters, the degree to which neighbouring plants profit from these investments, and the extent to which other plants in the environment invest or harbour profitable prey. Possibilities for indirect plant defence to arise from coevolution are discussed.

Cross‐correlation analysis of fluctuations in local populations of pear psyllids and anthocorid bugs

1. To test whether predatory anthocorids migrate into pear orchards when populations of pear psyllids are building up, a cross‐correlation analysis was carried out on their population numbers. Predator and prey population sizes were assessed weekly in 3 consecutive years (1991–93) by sampling pear leaves for eggs and nymphs of psyllids and pear tree branches for adult psyllids, as well as adults and nymphs of predatory anthocorids. The time‐series consisted of numbers (per leaf or branch) averaged over preselected pear trees in an orchard and, in addition, over other trees selected along the hedgerows flanking the orchard.

Leaf volatiles and polyphenols in pear trees infested by Psylla pyricola. Evidence of simultaneously induced responses

SummaryFeeding by the homopteranPsylla pyricola on leaves of pear trees induces the production of volatile compounds, such as (E,E)-α-farnesene and methyl-salicylate, as well as the production of polyphenols. The inference on induction is based on GC-MS and HPLC chromatograms from the same samples ofPsylla infested leaves, leaves from the same pear tree beforePsylla infestation and uninfested leaves from other pear trees.Psylla infestation greatly enhanced the production of volatiles ((E,E)-α-farnesene, methyl-salicylate and others) and triggered the production of new polyphenols, characterized by much longer retention times.However, the responses to infestation depend critically on leaf age (defined by leaf distance to apex). With respect to the leaf volatiles it appears that infested, old leaves produce fewer compounds and lower amounts of the volatiles than infested, young leaves. Moreover, there seem to be differences in pattern. Relative to (E,E)-α-farnesene, methyl-salicylate was found in much lower amounts in heavily infested, old leaves. With respect to polyphenols it was found that infested old leaves collected in August have polyphenols with the same retention times, but more or less equal amounts as uninfested young leaves collected in May. This shows thatPsylla infestation causes the induced response mostly in young leaves.The induced leaf volatiles may act as synomones to heteropteran bugs. As shown elsewhere,Anthocoris nemoralis responds significantly to (E,E)-α-farnesene and methyl-salicylate when offered in pure form against clean air in a Y-tube olfactometer. The effect of polyphenols on the performance ofP. pyricola is not yet known. Hence, a role in direct defence is still to be investigated.