Maurice W. Sabelis

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.

How plants obtain predatory mites as bodyguards

Phytophagous mites are a serious threat to their host plants; in absence of predators they tend to overexploit their food source. To prevent such a crash and maintain as much leaf area as possible host plants may defend themselves in various ways, one of which is to increase the effectiveness of natural enemies of the phytophagous mites. Predatory mites are considered to be very important natural enemies of plant-feeding mites and there is evidence for a mutualistic interaction with plants. Examples of how plants obtain and arrest predatory mites as bodyguards are discussed. It is known for a long time that some plant species provide pollen that appear to be a very profitable food source for some species of predatory mites: it does not only promote survival, but also allows development and egg production. In doing so, plants ensure themselves of bodyguards even before any damage is inflicted. Recently, evidence has been obtained that plants under attack by spider mites provide information by releasing a blend of volatile chemicals that are helpful to predatory mites in locating their prey. Plant-predator interactions are not always of a mutualistic nature. Some plant species invest in a rigorous defence against spider mites, even though this may be to the detriment of the predators: glandular hairs of some plant species entrap not only spider mites, but also their predators. The evolutionary implications of these various plant-predator interactions are discussed.

The dynamics of multiple infection and the evolution of virulence

While for pathogen clones singly occupying a host it may pay to adopt a relatively avirulent host exploitation strategy, clones sharing a host have a conflict of interest that favors more virulent strategies. As the number of infections per host depends on the force of infection and the force of infection, in turn, depends on prevailing virulence, evolutionary analysis needs to be integrated with population dynamics. A full-fledged approach requires exceedingly large capacities for bookkeeping of the infection events and is therefore difficult to establish. In this article the host-pathogen interaction is studied for the simple case in which hosts may become at most doubly infected. It appears that evolution and population dynamics give rise to a feedback mechanism. When double infections are frequent, increased virulence is favored; but when pathogens become more virulent, the force of infection will decrease, favoring lower virulence again. Thus, evolutionarily stable strategy (ESS) virulence depends on the interaction within hosts as well as on the interaction at the population level. As current models of host-microparasite interactions take only first infections into account, they may be inappropriate for evolutionary analyses, which would require modeling of within-host competition between strains and thus of multiple infections.

Differential Timing of Spider Mite-Induced Direct and Indirect Defenses in Tomato Plants

Through a combined metabolomics and transcriptomics approach we analyzed the events that took place during the first 5 d of infesting intact tomato (Lycopersicon esculentum) plants with spider mites (Tetranychus urticae). Although the spider mites had caused little visible damage to the leaves after 1 d, they had already induced direct defense responses. For example, proteinase inhibitor activity had doubled and the transcription of genes involved in jasmonate-, salicylate-, and ethylene-regulated defenses had been activated. On day four, proteinase inhibitor activity and particularly transcript levels of salicylate-regulated genes were still maintained. In addition, genes involved in phospholipid metabolism were up-regulated on day one and those in the secondary metabolism on day four. Although transcriptional up-regulation of the enzymes involved in the biosynthesis of monoterpenes and diterpenes already occurred on day one, a significant increase in the emission of volatile terpenoids was delayed until day four. This increase in volatile production coincided with the increased olfactory preference of predatory mites (Phytoseiulus persimilis) for infested plants. Our results indicate that tomato activates its indirect defenses (volatile production) to complement the direct defense response against spider mites.

Alternative Food, Switching Predators, and the Persistence of Predator‐Prey Systems

Sigmoid functional responses may arise from a variety of mechanisms, one of which is switching to alternative food sources. It has long been known that sigmoid (Holling’s Type III) functional responses may stabilize an otherwise unstable equilibrium of prey and predators in Lotka‐Volterra models. This poses the question of under what conditions such switching‐mediated stability is likely to occur. A more complete understanding of the effect of predator switching would therefore require the analysis of one‐predator/two‐prey models, but these are difficult to analyze. We studied a model based on the simplifying assumption that the alternative food source has a fixed density. A well‐known result from optimal foraging theory is that when prey density drops below a threshold density, optimally foraging predators will switch to alternative food, either by including the alternative food in their diet (in a fine‐grained environment) or by moving to the alternative food source (in a coarse‐grained environment). Analyzing the population dynamical consequences of such stepwise switches, we found that equilibria will not be stable at all. For suboptimal predators, a more gradual change will occur, resulting in stable equilibria for a limited range of alternative food types. This range is notably narrow in a fine‐grained environment. Yet, even if switching to alternative food does not stabilize the equilibrium, it may prevent unbounded oscillations and thus promote persistence. These dynamics can well be understood from the occurrence of an abrupt (or at least steep) change in the prey isocline. Whereas local stability is favored only by specific types of alternative food, persistence of prey and predators is promoted by a much wider range of food types.

Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato.

The tomato (Lycopersicon esculentum) mutant def-1, which is deficient in induced jasmonic acid (JA) accumulation upon wounding or herbivory, was used to study the role of JA in the direct and indirect defense responses to phytophagous mites (Tetranychus urticae). In contrast to earlier reports, spider mites laid as many eggs and caused as much damage on def-1 as on wild-type plants, even though def-1 lacked induction of proteinase inhibitor activity. However, the hatching-rate of eggs on def-1 was significantly higher, suggesting that JA-dependent direct defenses enhanced egg mortality or increased the time needed for embryonic development. As to gene expression, def-1 had lower levels of JA-related transcripts but higher levels of salicylic acid (SA) related transcripts after 1 d of spider mite infestation. Furthermore, the indirect defense response was absent in def-1, since the five typical spider mite-induced tomato-volatiles (methyl salicylate [MeSA], 4,8,12-trimethyltrideca-1,3,7,11-tetraene [TMTT], linalool, trans-nerolidol, and trans-β-ocimene) were not induced and the predatory mite Phytoseiulus persimilis did not discriminate between infested and uninfested def-1 tomatoes as it did with wild-type tomatoes. Similarly, the expression of the MeSA biosynthetic gene salicylic acid methyltransferase (SAMT) was induced by spider mites in wild type but not in def-1. Exogenous application of JA to def-1 induced the accumulation of SAMT and putative geranylgeranyl diphosphate synthase transcripts and restored MeSA- and TMTT-emission upon herbivory. JA is therefore necessary to induce the enzymatic conversion of SA into MeSA. We conclude that JA is essential for establishing the spider mite-induced indirect defense response in tomato.

HABITAT STRUCTURE AFFECTS INTRAGUILD PREDATION

Intraguild predation is thought to be ubiquitous in natural food webs. Yet, theory on intraguild predation predicts the intraguild prey to persist only under limited conditions. This gap between theory and empirical observations needs scrutiny. One reason might be that theory has focused on equilibrium dynamics and a limited set of species (usually three) that interact in well-mixed populations in unstructured habitats, and these assumptions will often not hold in natural systems. In this review, we focus on the effects of habitat structure on intraguild predation. Habitat structure could reduce encounter rates between predators and prey and could create refuges for prey. In both cases, habitat structure could reduce the strength of intraguild interactions, thereby facilitating species coexistence. A meta-analysis of studies on manipulation of habitat structure shows that intraguild prey indeed suffer less from intraguild predation in structured habitats. This was further confirmed by a meta-analysis in which studies on intraguild predation were classified according to habitat structure. Intraguild predation reduced densities of the intraguild prey significantly more in habitats with little structure than in habitats rich in structure. The effect of intraguild predation on the shared prey was negative, and not significantly affected by habitat structure. We conclude that habitat structure may increase persistence of the intraguild prey by decreasing the strength of the interaction between intraguild predator and intraguild prey.

HOW PLANTS BENEFIT FROM PROVIDING FOOD TO PREDATORS EVEN WHEN IT IS ALSO EDIBLE TO HERBIVORES

It is well established that plants provide alternative foods to predators of herbivorous arthropods. This provision may facilitate protection against herbivory. However, plants often cannot prevent other organisms from utilizing these foods as well. There are many examples of herbivorous arthropods that can feed on plant-provided foods such as extrafloral nectar and pollen. The question therefore arises whether individual plants still gain protection when not only the predators, but also the herbivores, can feed on these foods. We investigated this question using a mathematical model and experiments that assessed the impact of supplementary pollen on the dynamics of predatory mites (Iphiseius degenerans (Berlese)) and herbivorous thrips (Frankliniella occidentalis (Pergande)), two arthropods capable of using pollen for reproduction. Replicated greenhouse experiments showed that addition of pollen every two weeks to one young mature leaf of a male-sterile cucumber plant increased predator population growth...

Habitat structure and population persistence in an experimental community.

Understanding spatial population dynamics is fundamental for many questions in ecology and conservation. Many theoretical mechanisms have been proposed whereby spatial structure can promote population persistence, in particular for exploiter–victim systems (host–parasite/pathogen, predator–prey) whose interactions are inherently oscillatory and therefore prone to extinction of local populations. Experiments have confirmed that spatial structure can extend persistence, but it has rarely been possible to identify the specific mechanisms involved. Here we use a model-based approach to identify the effects of spatial population processes in experimental systems of bean plants (Phaseolus lunatus), herbivorous mites (Tetranychus urticae) and predatory mites (Phytoseiulus persimilis). On isolated plants, and in a spatially undivided experimental system of 90 plants, prey and predator populations collapsed; however, introducing habitat structure allowed long-term persistence. Using mechanistic models, we determine that spatial population structure did not contribute to persistence, and spatially explicit models are not needed. Rather, habitat structure reduced the success of predators at locating prey outbreaks, allowing between-plant asynchrony of local population cycles due to random colonization events.

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.