Jan Bruin

PLANT STRATEGIES OF MANIPULATING PREDATOR- PREY INTERACTIONS THROUGH ALLELOCHEMICALS: PROSPECTS FOR APPLICATION IN PEST CONTROL

To understand the role of allelochemicals in predator-prey interactions it is not sufficient to study the behavioral responses of predator and prey. One should elucidate the origin of the allelochemicals and be aware that it may be located at another trophic level. These aspects are reviewed for predator-prey interactions in general and illustrated in detail for interactions between predatory mites and herbivorous mites. In the latter system there is behavioral and chemical evidence for the involvement of the host plant in production of volatile allelochemicals upon damage by the herbivores with the consequence of attracting predators. These volatiles not only influence predator behavior, but also prey behavior and even the attractiveness of nearby plants to predators. Herbivorous mites disperse away from places with high concentrations of the volatiles, and undamaged plants attract more predators when previously exposed to volatiles from infested conspecific plants rather than from uninfested plants. The latter phenomenon may well be an example of plant-to-plant communication. The involvement of the host plant is probably not unique to the predator-herbivore-plant system under study. It may well be widespread since it makes sense from an evolutionary point of view. If so, prospects for application in pest control are wide open. These are discussed, and it is concluded that crop protection in the future should include tactics whereby man becomes an ally to plants in their strategies to manipulate predator-prey interactions through allelochemicals.

Plant-provided food for carnivorous insects : a protective mutualism and its applications

Plants provide insects with a range of specific foods, such as nectar, pollen, and food bodies. In exchange, they may obtain various services from arthropods. The role of food rewards in the plant–pollinator mutualism has been broadly covered. This book addresses another category of food-mediated interactions, focussing on how plants employ foods to recruit arthropod ‘‘bodyguards’’ as a protection against herbivores.

Plants are better protected against spider-mites after exposure to volatiles from infested conspecifics

When infested by herbivorous mites, cotton seedlings produce volatile cues that elicit attraction of predatory mites. Experiments were carried out to elucidate how downwinduninfested conspecific seedlings are affected by these volatiles. It was found that the rate of oviposition of herbivorous mites was reduced on seedlings exposed to volatiles from infested seedlings. Moreover, predatory mites were attracted by exposeduninfested seedlings. These results strongly suggest that uninfested plants are better protected against herbivore attack when exposed to airborne chemicals released by their infested neighbours.

Chemical information transfer between plants: back to the future

Chemical information conveyance between organisms has been well established for a wide range of organisms including protozoa, invertebrates, vertebrates and plant-parasitic plants. During the past 20 years, various studies have addressed whether chemical information conveyance also occurs between damaged and undamaged plants and many interesting pieces of evidence have been presented. To date, this research field has been restricted to the question whether and how plants (in general) are involved in plant-to-plant communication. However, apart from mechanistic questions, evolutionary questions should be addressed asking why plants do (or do not) exploit their neighbours information and whether their strategy is affected by e.g. environmental conditions or previous experience. Recent progress in the field of chemical information conveyance between damaged and undamaged plants warrants an intensified study of this exciting topic in chemical ecology.

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.

Predators use volatiles to avoid prey patches with conspecifics

1. Simple models of optimal foraging, such as ideal free distribution models, are based on the assumption that foragers are omniscient with respect to the quality of all patches in the environment; they know how much food and how many competitors are present in each patch. 2. In contrast, simple population dynamic models treat predator-prey distributions in a phenomenological way, and do not take fitness consequences for individual foragers into account. Yet, the precise way in which these distributions come into being is what really matters to population dynamics. It is therefore necessary to study the behavioural mechanisms underlying the distributions of foragers over patches. 3. We studied the behaviour of a predatory mite, Phytoseiulus persimilis, in response to prey patches occupied by conspecifics. It is well known that high predator densities in prey patches promote dispersal of these predatory mites. Our question was to what extent predators can assess the presence of conspecifics from a distance. 4. Experiments with a Y-tube olfactometer showed that predatory mites avoid patches occupied by conspecifics. 5. This avoidance cannot be attributed to odours of conspecific predators, or of prey damaged by predation, as these odour sources both appear to be attractive. 6. Separating the prey patch from the conspecific predators in the odour source led to the avoidance response only when the predators in the odour source were positioned upwind from the prey patch, and not when they were positioned downwind. This suggests that predators release an odour that elicits the production of yet another odour by the prey. This was supported by the observation that removal of adult prey led to a quick disappearance of the avoidance response. 7. We argue that distant discrimination between patches with and without competing conspecifics may be quite common among predators and parasitoids, and that the use of odours instead of physical inspection of patches allows predators to instantaneously integrate information on the distribution of food and competitors. 8. This behavioural mechanism may bring predators and parasitoids closer to behaving as ideal free foragers than was previously thought possible.

Do plants tap SOS signals from their infested neighbours

Ecologist have not been able to show unambigous evidence for the involvement of plant-to-plant signal transfer in the defence strategies of plants. However, phytopathologists and plant physiologists recently demonstrated that resistance in undamaged plants can be elicited by volatiles of plant origin. Now that empirical evidence is accumulating, there is every reason to ask why plants use the available information on the infestion status of their neighbours and to assess the fitness advantages associated with the tuning of their defence. The debate on the ecological and evolutionary significance of interplant communication needs to be revived.

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.

Host race formation in Tetranychus urticae: genetic differentiation, host plant preference, and mate choice in a tomato and a cucumber strain

The two‐spotted spider mite, Tetranychus urticae Koch, occurs in two colour forms in greenhouses in the Netherlands: a red form on tomato and a green form on cucumber. The evolutionary status of these strains was analysed by studying genetic differentiation, host plant preference, and mate choice. Males of the tomato strain preferred the female (30 h‐old) teleiochrysales from the same strain to those of the cucumber strain, independent of the host plants (tomato, cucumber, bean) on which the teleiochrysales were placed. In contrast, males of the cucumber strain were not selective. In a Y‐tube olfactometer, females of the cucumber strain were not responsive to host plant volatiles alone. However, in two‐choice disc experiments, where females were exposed to both volatile and contact cues, they settled on cucumber leaves in preference to tomato leaves. Females of the tomato strain preferred the odour of tomato leaves and settled on tomato leaves in preference to cucumber leaves. These experimental results provide the first evidence for (1) host‐plant independent mate selection in male spider mites and (2) olfactory discrimination between host plants in female spider mites.

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.