Information use by the predatory mite Phytoseiulus persimilis (Acari ...

Appl. Entomol. Zool. 40 (1): 1–12 (2005)

Review

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Information use by the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae), a specialised natural enemy of herbivorous spider mites Jetske G. DE BOER* and Marcel DICKE Laboratory of Entomology, Wageningen University; P.O. Box 8031, 6700 EH Wageningen, The Netherlands (Received 5 April 2004; Accepted 1 June 2004)

Abstract Plants can respond to infestation by herbivores with the emission of specific herbivore-induced plant volatiles. Many carnivorous arthropods that feed on herbivorous prey use these volatiles to locate their prey. Despite the growing amount of research papers on the interactions in tritrophic systems, it has remained unclear how carnivorous arthropods use herbivore-induced plant volatiles in prey-location. We investigated three important aspects of information use by the predatory mite Phytoseiulus persimilis, a specialised natural enemy of herbivorous spider mites. First, we showed that the foraging efficiency of predatory mites was not hampered by the presence of volatiles induced by nonprey caterpillars on brussels sprouts plants. Second, we revealed an important role for the volatile compound methyl salicylate. Predatory mites appear to use the presence of this compound, rather than its relative contribution to a volatile blend, to discriminate between two volatile blends. Third, we demonstrated that the role of methyl salicylate in the foraging behaviour of P. persimilis depends on previous experiences of the predators with this compound. Our research improves the understanding of the selection pressures that act on the foraging responses of carnivorous arthropods, and consequently on the selection pressures on volatile emission by plants in response to herbivory. Key words: Tritrophic systems; food webs; herbivore-induced plant volatiles; methyl salicylate; foraging behaviour

plants by the predatory mite Phytoseiulus persimilis, a specialised natural enemy of herbivorous spider mites. Carnivores that feed on herbivorous prey can use information from different sources to locate their victims: information from the prey itself or information from the prey’s food plant. It is now widely accepted that plants provide an important source of information to natural enemies of herbivorous arthropods. Arthropod herbivores are only small components in the environment and they are under strong selection not to reveal themselves (e.g., Turlings et al., 1991; Vet and Dicke, 1992; Du et al., 1996). Plants, on the other hand, are much larger than herbivorous arthropods and are therefore easier to detect. Moreover, plants emit specific information in response to herbivory, i.e. herbivore-induced plant volatiles (e.g., Dicke et al., 1990a; Turlings et al., 1990; Vet and Dicke, 1992; Takabayashi and Dicke, 1996). This ability has been shown for many plant species in a range of

INTRODUCTION Information mediates all interactions between organisms, such as finding mates and food, or avoiding competitors and predators. Information can be visual, chemical, auditory or tactile. An important aspect of information use is discrimination of relevant signals from background noise. This idea is easy to grasp for auditory cues: it is harder to hear someone in a loud discotheque than in a quiet restaurant. Similarly, natural background noise can influence the ability of female frogs to discriminate between the advertisement calls of different conspecific males (Wollerman and Wiley, 2002). The same applies to chemical cues. In their use of chemical information, animals need to filter out the relevant signals from the irrelevant background noise; for example predators need to discriminate between cues related to prey and cues that are not related to suitable prey. The topic of this paper is the use of chemical information from

* To whom correspondence should be addressed at: E-mail: [email protected] DOI: 10.1303/aez.2005.1

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J. G. DE BOER and M. DICKE

plant families, including Brassicaceae, Cucurbitaceae, Fabaceae, and Solanaceae (e.g. Dicke, 1999; Dicke and Vet, 1999). Herbivore-induced plant volatiles are used as foraging cues by a diverse range of arthropod carnivore species, including parasitoid wasps, and predatory bugs and mites (e.g. Sabelis and Van de Baan, 1983; Dicke et al., 1990a; Turlings et al., 1990; Steinberg et al., 1992; Shimoda et al., 1997; Scutareanu et al., 1997; Van Loon et al., 2000a). These carnivores can reduce the herbivore pressure on plants and thereby have a positive effect on plant fitness (Dicke and Sabelis, 1989; Van Loon et al., 2000b; Fritzsche Hoballah and Turlings, 2001). Both plants and carnivores can thus benefit from herbivore-induced plant volatiles and therefore it can be expected that plants are under selection to emit a signal that attracts effective carnivores, while the carnivores, in turn, are under selection to optimise their responses to these plant signals (Vet, 1999a). Despite the rapidly growing number of research articles on the interactions in tritrophic systems, it has remained unknown how carnivorous arthropods use herbivore-induced plant volatiles to locate their prey. To narrow this gap in the existing knowledge, we have studied a tritrophic system consisting of the predatory mite Phytoseiulus persimilis, spider mites Tetranychus urticae, and lima bean plants (Phaseolus lunatus). This tritrophic system was one of the first systems in which the use of herbivore-induced plant volatiles by natural enemies of herbivorous arthropods has been demonstrated (Dicke et al., 1990a). Since then, it has been an important model system for research on the responses of carnivores to plant volatiles and on the mechanisms of volatile-induction in plants (e.g. Takabayashi and Dicke, 1996; Dicke et al., 1999; Koch et al., 1999; Ozawa et al., 2000a; Horiuchi et al., 2003). We have addressed three questions that had received little attention so far: (i) Can predators use volatiles induced by suitable prey herbivores in an environment with a background of other plant volatiles? (ii) Which parts of a volatile blend signal the presence of suitable prey herbivores to predators? (iii) Does learning play a role in the foraging responses of predatory arthropods? In the following three paragraphs, we discuss each of these questions.

FORAGING IN AN ENVIRONMENT WITH NON-PREY HERBIVORES To date most studies on the responses of predators to herbivore-induced plant volatiles have been carried out in the laboratory in an odour-free background (Sabelis et al., 1999; Hunter, 2002; but see Drukker et al., 1995; Shimoda et al., 1997; DeMoraes et al., 1998; Thaler, 1999; Geervliet et al., 2000; and Kessler and Baldwin, 2001 for field studies). Under natural conditions, however, predators have to locate their prey in an environment where a diversity of other information is available as well. In the field, plants are part of a community, in which most plants emit a blend of volatiles that can be induced by herbivory, or by other biotic or abiotic factors. Wind turbulence can mix the volatiles emitted by two or more neighbouring plants and thereby create variation in the information that is available to a foraging carnivore. In addition, more than one herbivore species can simultaneously infest the same individual plant, and this presumably influences the composition of the volatile blend (Shiojiri et al., 2001; RodriguezSaona et al., 2003). There is only limited knowledge on the responses of carnivores to the preyrelated signal when variation in information is caused by the presence of non-prey herbivores on heterospecific or conspecific plants (odour mixing), or on the same individual plant (multiple infestation) (but see Monteith, 1960; Shiojiri et al., 2000, 2001, 2002; Vos et al., 2001; Gohole et al., 2003a, b; Perfecto and Vet, 2003; Rodriguez-Saona et al., 2003). Background noise of volatiles induced by non-prey herbivores, through odour mixing or multiple infestation, may reduce the detectability of the signal that is used by carnivores to locate their prey, or hamper the ability of carnivores to discriminate between relevant and irrelevant information. Hence, the probability that carnivores are able to locate their prey may be influenced by background noise. We investigated how the attraction of P. persimilis to volatiles induced by their prey was influenced by volatiles from Pieris brassicae-infested brussels sprouts plants (Dicke et al., 2003a). Pieris brassicae is not suitable as prey for P. persimilis, and brussels sprouts plants are poor host plants for spider mites. Mixing the volatiles from T. urticaeinfested lima bean plants with the volatiles from P.

Information Use by Phytoseiulus persimilis

brassicae-infested brussels sprouts did not result in a reduced attraction of P. persimilis to T. urticae-induced volatiles in the Y-tube olfactometer (Fig. 1). Besides the olfactometer, we used a greenhouse set-up that resembled the situation in the field more closely, with intact plants standing in soil (Pallini et al., 1997; Janssen, 1999; Dicke et al., 2003a). This experiment confirmed that the foraging efficiency of predatory mites was not hampered by the presence of P. brassicae-infested brussels sprouts plants (Dicke et al., 2003a). Analysis of the chemical composition of the volatile blends from T. urticae-infested plants and brussels sprouts plants infested with the non-prey caterpillar P. brassicae showed that the degree of overlap between the volatile blends is low (Mattiacci et al., 1994; Dicke et al., 1999). Moreover, P. persimilis was not attracted to the volatiles from P. brassicae-infested brussels sprouts plants (Dicke et al., 2003a). This may indicate that the volatiles emitted by P. brassicae-infested brussels sprouts plants do not play a role in the foraging behaviour of P. persimilis and therefore do not disturb its foraging efficiency when mixed with volatiles from prey-infested bean plants. Results from Gohole et al. (2003a, b) support this idea. The stemborer par-

Fig. 1. Effect of mixing the volatiles from Tetranychus urticae-infested lima bean leaves with the volatiles from Pieris brassicae-infested brussels sprouts leaves on the foraging responses of the predatory mite Phytoseiulus persimilis. The white bar presents the choice of predatory mites between two equal sets of 9 lima bean leaves infested with 50 T. urticae per leaf. The black bar presents the choice of predatory mites between the same two sets of lima bean leaves but one of them was combined with 3 brussels sprouts leaves infested with 50 P. brassicae larvae per leaf. Numbers in bars represent the total numbers of predators choosing for each odour source. Predatory mites had been reared on spider mites on lima bean and they had been individually kept in Eppendorf vials without food for 24 h prior to testing. A 22 contingency table was used to compare the distribution of predatory mites over the odour sources in the two situations (n.s. p0.05). Modified from Dicke et al. (2003a).

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asitoid Cotesia sesamiae is strongly attracted by volatiles from uninfested molasses grass, while the parasitoid Dentichasmias busseolae is repelled (Khan et al., 1997; Gohole et al., 2003a, b). The responses of C. sesamiae to stemborer-induced maize volatiles were hampered in a background of molasses grass odour, while the responses of D. busseolae were not. To conclude, our study on odour mixing implies that herbivore-induced plant volatiles can benefit spider mite-infested plants by attracting predatory mites, and can benefit P. persimilis in prey location in more complex situations than investigated so far, i.e. in a system with non-prey caterpillars. Currently, we are investigating how the foraging behaviour of P. persimilis is affected when the volatiles from T. urticae-infested plants are mixed with the volatiles from other plant-herbivore-complexes, which emit volatile blends that are more similar to the blend from T. urticae-infested lima bean plants, or when two herbivore species attack a single plant simultaneously. IDENTIFYING THE SIGNAL THAT ENABLES CARNIVORES TO DISCRIMINATE BETWEEN TWO VOLATILE BLENDS Blends of herbivore-induced plant volatiles consist of mixtures of compounds, some of which are passively released and some of which are synthesised de novo upon herbivory (Paré and Tumlinson, 1997). Several factors influence the composition of the blends of volatiles released by herbivore-damaged plants: plant species or genotype, plant tissue and age, time of the day, herbivore species and developmental stage, attack by a second herbivore species or pathogen, and abiotic factors (e.g. Takabayashi et al., 1991, 1994, 1995; Turlings et al., 1993, 1995, 1998; Loughrin et al., 1994, 1995; Geervliet et al., 1997; DeMoraes et al., 1998; Dicke, 1999; Halitschke et al., 2000; Maeda et al., 2000; Shiojiri et al., 2001; Cardoza et al., 2002; Fritzsche Hoballah et al., 2002; Gouinguené and Turlings, 2002; Schmelz et al., 2003; Van den Boom et al., 2004). For carnivores it is especially important to respond to the signal that identifies the presence of suitable herbivores feeding on a plant. It seems unlikely that the composition of the complete blend of volatiles emitted by a herbivoreinfested plant constitutes the prey-location signal

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for foraging carnivores because these blends can consist of more than a hundred different compounds. Moreover, the composition of the volatile blend of a specific plant-herbivore combination can vary, e.g. when a second herbivore species infests the same individual plant, or with different abiotic conditions to which the plant is exposed. Hence, we assume that the information—the herbivore-induced plant volatile blend—that is available to a foraging carnivore includes both a signal part (related to the presence of suitable prey) and a noise part (not related to the presence of suitable prey). However, it is not yet known which parts of the volatile blends constitute the signal that reveals the presence of prey to carnivores, and which parts are noise (e.g. Chadwick and Goode, 1999; Vet, 1999b; Dicke and Van Loon, 2000; Degenhardt et al., 2003). In identifying which specific compounds play a role in the foraging responses of carnivores, a comparison of the behavioural preferences of carnivores with the chemical composition of volatile blends can pinpoint potentially bioactive compounds. However, in doing so, two problems can arise. First, the sensitivity of the analytical equipment used to determine the composition of a blend of herbivore-induced plant volatiles is much lower than the sensitivity of the chemoreceptors of the arthropods themselves (e.g. Pickett et al., 1998). The absence of a compound in a volatile blend as measured with GC-MS (gas chromatography–mass spectrometry) is thus no absolute proof that this specific compound is not emitted by a plant. This problem can partly be solved by a coupled analysis of volatile blend composition and electrophysiological recording of the perception of compounds by chemoreceptors of an arthropod (gas chromatography–electroantennography, or GC-EAG). This technique can be used to elucidate whether the plant emits compounds that are not detected by the GC but that are detected by the arthropod (Pickett et al., 1998). GC-EAG can also be used to narrow down the range of potentially bioactive compounds in the volatile blend by measuring the sensory responses of the arthropod to the different compounds in the volatile blend. However, although this technique has been used successfully for a long time to identify bioactive compounds for herbivores, it has been applied to carnivores only recently (Du et al., 1998; Van Loon and Dicke, 2000;

Weissbecker et al., 2000; Smid et al., 2002). It has proven to be particularly difficult with the predatory mite P. persimilis (De Bruyne et al., 1991). A second problem arises when the compounds that are potentially important in carnivore foraging are not commercially available or have not been identified yet. This obviously complicates further experiments. In identifying the role of specific volatile compounds in the foraging behaviour of P. persimilis, we avoided these problems by working with volatile blends of known composition, and manipulating the composition of these blends by adding synthetic compounds. Previous research had indicated that the compound methyl salicylate (MeSA) might play a role in the foraging behaviour of P. persimilis (Dicke et al., 1999a). Dicke et al. (1999) compared the attractiveness of two volatile blends from lima bean plants, one induced by infestation with T. urticae, and the other by treatment with the plant hormone jasmonic acid (JA). Although both volatile blends attracted P. persimilis, in a choice-test predatory mites preferred the volatiles from T. urticaeinfested lima bean plants to those from JA-treated plants (Dicke et al., 1999; see also Fig. 2A). The composition of both volatile blends is similar, but MeSA is only emitted upon infestation with T. urticae, and not upon treatment with JA (Dicke et al., 1999). We showed that predatory mites can indeed use the presence of MeSA in the volatile blend from T. urticae-infested lima bean plants to discriminate between T. urticae-infested and JAtreated lima bean plants (De Boer and Dicke, 2004a). After adding synthetic MeSA to the JA-induced volatile blend, the predators lost their preference for the volatiles from T. urticae-infested lima bean plants (Fig. 2A). A qualitative difference in the presence of MeSA thus had a significant effect on the foraging responses of P. persimilis. In contrast, a quantitative difference in the amount of MeSA did not affect the choice of the predators between two odour sources (Fig. 2B). We tested this by offering predatory mites a choice between two T. urticae-induced volatile blends from lima bean, one of which was combined with an extra dose of synthetic MeSA (De Boer and Dicke, 2004a). Predatory mites were attracted to the single compound MeSA in a dose-dependent way (De Boer and Dicke, 2004a) but apparently this does not happen when MeSA is part of a complex blend of


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Fig. 2. Effect of methyl salicylate (MeSA) on the choices of predatory mites between two volatile blends. (A) Effect of qualitative difference in methyl salicylate: black bar represents the choice of predators between 4 lima bean leaves infested with 50 spider mites per leaf and 4 lima bean leaves treated with jasmonic acid (JA, 1 mM); white bar represents the choice of predators between the same two sets of leaves when 0.2 m g MeSA was added to the volatiles from the JA-treated leaves. (B) Effect of quantitative difference in methyl salicylate: black bar represents the choice of predators between two equal sets of 4 lima bean leaves infested with 50 spider mites per leaf; white bar represents the choice of predators between the same two sets of leaves when one of them was combined with 0.2 m g MeSA. Numbers in bars present the total number of predators choosing for each odour source. All predators had been reared on spider mites on lima bean and had been kept individually in an Eppendorf vial without food for 1–3 h before testing. A generalized linear model (McCullagh and Nelder, 1989) was used to analyse the effect of adding MeSA (n.s. p0.05; *** p0.001). In (A) the choice of predatory mites between the odour sources was analysed with a two-sided binomial test (*** p0.001). Modified from De Boer and Dicke (2004a).

spider mite-induced lima bean volatiles. Furthermore, we demonstrated recently that P. persimilis does not even discriminate between the single compound MeSA and the complete natural volatile blend induced by T. urticae on lima bean (De Boer et al., 2004), thus supporting the important role for MeSA in the foraging behaviour of P. persimilis. In conclusion, our experiments demonstrated an important role for MeSA in the foraging behaviour of P. persimilis. It remains to be investigated whether this finding applies to our specific tritrophic system of lima bean plants, T. urticae, and the predatory mite P. persimilis, or whether it applies to a broader range of plant species and nonprey herbivore species, or even to other tritrophic systems. To date, the volatile blends released upon T. urticae-infestation from at least 16 plant species from 8 different families have been analysed, and 13 of them emitted MeSA (Dicke et al., 1990a; Takabayashi et al., 1991, 1994; Krips et al., 1999; Ozawa et al., 2000a, b; Maeda and Takabayashi, 2001; Van den Boom et al., 2004). However, MeSA is also commonly found in the volatile blends of plants infested with other herbivore

species that are not suitable as prey for P. persimilis (e.g. Bolter et al., 1997; Van Poecke et al., 2001). It thus seems unlikely that predatory mites can always identify the presence of prey on a plant using MeSA only. In addition to MeSA, the predators most likely use other compounds as well. Several other studies have identified carnivoreattracting compounds from herbivore-induced volatile blends by testing their attractiveness as single compounds, as mixtures of synthetic compounds, or as fractions of the total volatile blend (e.g. Dicke et al., 1990a; Turlings et al., 1991; Whitman and Eller, 1992; Scutareanu et al., 1997; Du et al., 1998; Turlings and Fritzsche, 1999; Drukker et al., 2000b; Birkett et al., 2003). For example, Du et al. (1996, 1998) showed that the parasitoid Aphidius ervi prefers the volatiles from broad bean infested with the host aphid Acyrthosiphon pisum to the volatiles from broad bean plants infested with the non-host aphid Aphis fabae. The volatile blend induced by Ac. pisum includes 6-methyl-5-hepten-2-one, whereas this compound has not been detected in the blend induced by A. fabae. Because A. ervi is attracted to

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6-methyl-5-hepten-2-one, this suggests that A. ervi could use this compound to discriminate between the two blends. However, this was not explicitly demonstrated. No studies have previously investigated the role of specific volatile compounds within a natural volatile blend or demonstrated a role in enabling carnivorous arthropods to discriminate between two odour blends. Therefore, our results are the first evidence to demonstrate that specific compounds can play a significant role in enabling predatory mites to discriminate between two odour sources. PHENOTYPIC PLASTICITY IN THE FORAGING BEHAVIOUR OF P. PERSIMILIS The fact that information from plants infested with suitable prey herbivores displays temporal and spatial variation raises another important question: how can carnivores adapt their responses to these cues? Genetic adaptations to the information could include increased perception of the signal, more efficient processing of information or decision making, and enhanced discrimination between signal and noise (Vet, 1999a). Studies on genetic adaptation in the responses of carnivores to herbivore-induced plant volatiles have been initiated recently, and genetic variation has been demonstrated for the predatory mites Amblyseius womersleyi and P. persimilis, and the parasitoid wasp Cotesia glomerata (Margolies et al., 1997; Maeda et al., 1999, 2001; Jia et al., 2002; Wang et al., 2003). Besides genetic adaptation, phenotypic plasticity can enable carnivores to cope with variation in prey-location cues; between as well as within generations of carnivores (e.g. Via, 1987; Dukas, 1998). Phenotypic plasticity in responses to herbivore-induced plant volatiles has been well-studied for parasitoid wasps (reviewed by Turlings et al., 1993; Vet et al., 1995). These wasps can learn to associate a specific volatile blend to the presence of a specific host herbivore, for example when they are exposed to this information during oviposition in the host. Studies to investigate what parasitoids can learn have been initiated recently. Meiners et al. (2003) showed that by exposure to a mixture of three synthetic compounds in the presence of host frass the parasitoid Microplitis croceipes learned to respond to two of the individual components but not to the third one. When the parasitoid was exposed to the third com-

ponent as a single compound it did learn to respond, suggesting that the other components of the mixture inhibited or suppressed learning of the third component. Moreover, M. croceipes females could learn to discriminate between alcohols with a different chain length or position of the alcoholic group, but generalisations to structurally similar compounds also occurred (Meiners et al., 2002). Such generalisations have also been reported for Leptopilina heterotoma, a larval parasitoid of drosophilid fruit flies (Vet et al., 1998). Furthermore, Vet et al. showed that to differentiate between two odour sources that differed in the amount of only one compound, parasitoids had to experience one odour in a rewarding context and the other odour in a non-rewarding context. Associative learning enables parasitoids to temporarily specialise on the odours from the foodplants of their hosts in a certain place and time. In contrast to the studies on learning in parasitoid wasps, studies on learning of herbivore-induced plant volatiles by arthropod predators are still scarce (e.g. Bernays, 1993; Dicke et al., 1998). However, several studies have shown an effect of previous experiences with volatiles on the subsequent foraging responses of predators (e.g. Dicke et al., 1990b; Dwumfour, 1992; Takabayashi and Dicke, 1992; Krips et al., 1999). Moreover, Drukker et al. (2000a, b) reported that predators that had been reared in the absence of volatiles were only weakly attracted to prey-related information compered to predators that did have experience with these volatiles. We have investigated how the foraging responses of the predatory mite P. persimilis are influenced by previous experiences with volatiles, in particular with MeSA, the compound that plays an important role in the foraging behaviour of P. persimilis. To this end, we compared the responses of predatory mites that had been reared on spider mites on lima bean or cucumber plants. Cucumber plants do not emit MeSA upon spider mite-infestation whereas lima bean plants do, and thus, unlike lima bean-reared predators, cucumber-reared predators have not experienced MeSA (Takabayashi et al., 1994; Dicke et al., 1999). This difference in experience acquired during rearing indeed led to a difference in attraction to MeSA. In contrast to predators that had been reared on lima bean, cucumberreared predators were not attracted to MeSA (Fig.


3A; De Boer and Dicke, 2004b). We explicitly demonstrated that experience with MeSA caused the difference in attraction of lima bean-reared and cucumber-reared predators to MeSA by rearing a third group of predators on cucumber in the presence of synthetic MeSA. These MeSA-experienced predators were indeed attracted to MeSA (Fig. 3A; De Boer and Dicke, 2004b). There was also some effect of exposing the cucumber-reared predators to MeSA for three days during the adult phase on their response to MeSA. Experience with MeSA during rearing also influenced the choices of P. persimilis between two volatile blends that differed in the presence of MeSA: lima bean-reared predators preferred the volatiles from T. urticae-infested lima bean (including MeSA) to those of JA-treated lima bean (lacking MeSA), whereas cucumber-reared predators preferred the volatiles from JA-treated lima bean (Fig. 3B; De Boer and Dicke, 2004b). Predators that had been reared on cucumber in the presence of synthetic MeSA did not discriminate between these volatile blends. This result confirms that the choice of predators between these two odour sources partly depends on MeSA (see also Fig. 2A). However, the fact that the last group of predatory mites does not discriminate between the odour sources indicates that other compounds also play a role. For example, predatory mites that have been reared on spider mites on cucumber have experienced large amounts of (E)-b -ocimene (De Boer et al., unpublished data). This compound is also emitted in large amount by JA-treated lima bean plants but to a lesser extent by T. urticae-infested lima bean (Dicke et al., 1999). In conclusion, our results demonstrate that a small difference in the composition of the volatile blend that predatory mites experience during their juvenile development can have large effects on their subsequent foraging behaviour. A difference in the presence of only one compound (MeSA) can even explain the choice of P. persimilis between two odour sources that differ in the presence of this compound. However, compared to parasitoid wasps, predatory mites seem to need experience for a longer period before their behaviour is changed (Dicke et al., 1990b; Krips et al., 1999; Drukker et al., 2000a, b; De Boer and Dicke, 2004b). Several aspects of the biology and ecology of predatory mites may explain this. In contrast to many parasitoid wasp species that develop inside

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Fig. 3. The influence of experience with methyl salicylate (MeSA) on the role of this compound in the foraging behaviour of predatory mites. Black bars represent the choices of predatory mites that had been reared on spider mites on lima bean (which emits MeSA), white bars represent the choices of predators that had been reared on spider mites on cucumber (which does not emit MeSA), grey bars represent the choices of predators that had been reared on spider mites on cucumber in the presence of synthetic MeSA. All predators had been kept individually in an Eppendorf vial without food for 1–3 h before testing. (A) Attraction to the single compound MeSA (0.2 m g). (B) Choice between the volatiles from T. urticae-infested lima bean leaves (which emits MeSA) and JA-treated lima bean (which does not emit MeSA). Choices between odour sources were analysed with a two-sided binomial test (n.s. p0.05; * p0.05; ** p0.01; *** p0.001). Modified from De Boer and Dicke (2004b).

their host, predatory mites are exposed to volatiles induced by their prey during their entire development. Moreover, the development of predatory mites is hemimetabolous which may mean that the olfactory systems of immature stages and the adult phase resemble each other more than for different developmental stages of holometabolous carnivores, such as parasitoid wasps or flies. In fact, one study showed that the protonymphs of two species of predatory mites (including P. persimilis) were attracted to herbivore-induced volatiles (Dong and Chant, 1986), demonstrating that immature preda-

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tory mites can indeed perceive these cues and respond to them. Unlike parasitoid wasps, predatory mites are also predacious during the adult phase and adults respond to volatiles in search of both oviposition sites and food. Besides using herbivore-induced plant volatiles in long-distance searching of a new prey patch, predatory mites can also use these cues to remain in a prey patch by responding to the steep odour gradient at the border of the patch (Sabelis et al., 1984). The learned response to the volatiles emitted by the plant on which they develop probably helps predatory mites to optimise this response that prevents them from leaving a prey patch that has not been exterminated yet. However, when the predators start searching for a new prey patch, they may encounter prey on another plant species than the one on which they developed, and this novel plant species is likely to emit a different volatile blend in response to spider mite infestation (see for example Van den Boom et al., 2004). It has now been demonstrated that the responses of P. persimilis remain flexible during the adult phase. The adult predatory mites can still acquire experiences with volatiles and modify their responses accordingly (Drukker at al., 2000a; De Boer and Dicke, 2004b). Once predatory mites have found a new prey patch as adult, they will stay—and thus will be exposed to the volatiles emitted by the prey-infested plant—for relatively long periods compared to the period needed for an oviposition by a parasitoid wasp (Drukker et al., 2000a). This is likely to explain the relatively long period that it takes before the behaviour of predatory mites is modified because of such an experience, hours or days for predatory mites versus seconds or minutes for parasitoid wasps (e.g. Turlings et al., 1993; Vet et al., 1995). We expect that the learning abilities of predatory mites play a significant role in a natural environment where prey-location cues vary in time and space, and where nonprey herbivores are also present. Clearly, field experiments are needed to evaluate the role of learning under such natural conditions. FUTURE PERSPECTIVES To understand the ecology of induced indirect plant defences, it is essential to investigate the underlying machanisms (Dicke et al., 2003b). Understanding both ecological functions and the under-

lyng mechanisms will bring opportunities to manipulate plant-herbivore-carnivore systems so as to improve control of arthropod pests in an environmentally benign way. Our work led to important new insights in the understanding of information use by the specialised natural enemy of spider mites, P. persimilis: (i) Volatiles induced by non-prey caterpillars do not hamper the foraging behaviour of P. persimilis (Dicke et al., 2003a); (ii) Methyl salicylate plays an important role in the foraging responses of P. persimilis (De Boer and Dicke, 2004a); (iii) A small difference, i.e. in the presence of one compound, in the volatile blend that predatory mites experience during their juvenile development can determine the choice of the predators between two volatile blends (De Boer and Dicke, 2004b). An important next step is to investigate whether our findings apply to the foraging behaviour of P. persimilis in systems with other plant and herbivore species than we used here. Finally, predatory mites are important biocontrol agents in a range of crops and knowledge on their responses to volatiles from plants can contribute to the development of methods to manipulate their behaviour in the crop, and thereby to a more efficient control of pests (e.g. Degenhardt et al., 2003; Powell and Pickett, 2003). For example, crops may be selected or engineered that emit a larger amount of induced volatiles that are important in prey-location by the predators, or prior to releasing the predators in the crop they could be exposed to specific compounds that improve their searching efficiency. ACKNOWLEDGEMENTS We thank Wouter Tigges, Leo Koopman, Frans van Aggelen, André Gidding, and Bert Essenstam for rearing of spider mites and plants. JGDB was funded by the research council Earth and Life Sciences from the Dutch Science Foundation (NWO-ALW).

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