Phytoseiulus persimilis response to herbivore-induced plant volatiles as a function of mite-days

The predatory mite, Phytoseiulus persimilis (Acari: Phytoseiidae), uses plant volatiles (i.e., airborne chemicals) triggered by feeding of their herbivorous prey, Tetranychus urticae (Acari: Tetranychidae), to help locate prey patches. The olfactory response of P. persimilis to prey-infested plants varies in direct relation to the population growth pattern of T. urticae on the plant; P. persimilis responds to plants until the spider mite population feeding on a plant collapses, after which infested plants do not attract predators. It has been suggested that this represents an early enemy-free period for T. urticae before the next generation of females is produced. We hypothesize that the mechanism behind the diminished response of predators is due to extensive leaf damage caused by T. urticae feeding, which reduces the production of volatiles irrespective of the collapse of T. urticae population on the plant. To test this hypothesis we investigated how the response of P. persimilis to prey-infested plants is affected by: 1) initial density of T. urticae, 2) duration of infestation, and 3) corresponding leaf damage due to T. urticae feeding. Specifically, we assessed the response of P. persimilis to plants infested with two T. urticae densities (20 or 40 per plant) after 2, 4, 6, 8, 10, 12 or 14 days. We also measured leaf damage on these plants. We found that predator response to T. urticae-infested plants can be quantified as a function of mite-days, which is a cumulative measure of the standing adult female mite population sampled and summed over time. That is, response to volatiles increased with increasing numbers of T. urticae per plant or with the length of time plant was infested by T. urticae, at least as long at the leaves were green. Predatory mites were significantly attracted to plants that were infested for 2 days with only 20 spider mites. This suggests that the enemy-free period might only provide a limited window of opportunity for T. urticae because relatively low numbers of T. urticae per plant can attract predators. Leaf damage also increased as a function of mite-days until the entire leaf was blanched. T. urticae populations decreased at this time, but predator response to volatiles dropped before the entire leaf was blanched and before the T. urticae population decreased. This result supports our hypothesis that predator response to plant volatiles is linked to and limited by the degree of leaf damage, and that the quantitative response to T. urticae populations occurs only within a range when plant quality has not been severely compromised.     

Conditioned olfactory responses of a predatory mite, Neoseiulus womersleyi, to volatiles from prey-infested plants

To clarify the prey‐finding behavior of the predatory mite Neoseiulus womersleyi (Schicha) (Acari: Phytoseiidae), we studied its olfactory responses to volatiles from the prey‐infested plant on which the mites had been collected. We used a local N. womersleyi population called Kanaya collected from tea (Camellia sinensis L.) (Theaceae) plants infested by Tetranychus kanzawai Kishida (Acari: Tetranychidae) in Kanaya City, Japan. Neoseiulus womersleyi (Kanaya population) were more attracted to volatiles from tea plants infested with five female T. kanzawai per leaf for 7 days than to intact tea leaves in a Y‐tube olfactometer. Tetranychus kanzawai‐induced tea leaf volatiles were identified as (E)‐β‐ocimene, (E)‐4,8‐dimethyl‐1,3,7‐nonatriene, and (E,E)‐α‐farnesene. As olfactory responses are known to differ among local populations of N. womersleyi, we compared the responses of the Kanaya population with those of a Kikugawa population collected from tea plants infested by T. kanzawai in Kikugawa City. To test the influence of previous predation experience, we reared the two populations on tea plants infested by T. kanzawai or on kidney bean plants (Phaseolus vulgaris) infested by Tetranychus urticae Koch. The Kanaya population was more attracted to the volatiles from infested plants on which they had been reared. Because the Kanaya population was not attracted to the plant volatiles they had not previously experienced, the positive response to previously experienced volatiles might be the result of learning. By contrast, the Kikugawa population showed no preference for previously experienced volatiles from infested plants. The implications of this flexibility in foraging behavior are discussed.     

Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory

Plants infested with a single herbivore species can attract natural enemies through the emission of herbivore‐induced plant volatiles (HIPVs). However, under natural conditions plants are often attacked by more than one herbivore species. We investigated the olfactory response of a generalist predators Macrolophus caliginosus to pepper infested with two‐spotted spider mites, Tetranychus urticae, or green peach aphid, Myzus persicae, vs. plants infested with both herbivore species in a Y‐tube olfactometer set up. In addition, the constituents of volatile blends from plants exposed to multiple or single herbivory were identified by gas chromatography‐mass spectrometry (GC‐MS). The mirid bugs showed a stronger response to volatiles emitted from plants simultaneously infested with spider mites and aphids than to those emitted from plants infested by just one herbivore, irrespective of the species. Combined with results from previous studies under similar conditions we infer that this was a reaction to herbivore induced plant volatiles. The GC‐MS analysis showed that single herbivory induced the release of 22 additional compounds as compared with the volatiles emitted from clean plants. Quantitative analyses revealed that the amount of volatile blends emitted from pepper infested by both herbivores was significantly higher than that from pepper infested by a single herbivore. Moreover, two unique substances were tentatively identified (with a probability of 94% and 91%, respectively) in volatiles emitted by multiple herbivory damaged plants: α‐zingiberene and dodecyl acetate.     

Odour-mediated responses of a predatory mirid bug and its prey, the two-spotted spider mite

It has been shown that many natural enemies of herbivorous arthropods use herbivore induced plant volatiles (HIPVs) to locate their prey. Herbivores can also exploit cues emitted by plants infested with heterospecifics or conspecifics. A study was conducted to test whether green bean HIPVs as well as odours emitted directly by spider mites influenced the orientation behaviour of the predatory mirid bug, Macrolophus caliginosus and its prey, Tetranychus urticae in a Y-tube olfactometer. Our results show that both spider mites and M. caliginosus preferred spider mite infested green bean plants to uninfested plants. For M. caliginosus this response was mediated by HIPVs whereas for T. urticae it was mediated through a composite response to both HIPVs and odours emitted directly by the conspecifics (and their associated products). The results may be of use in practical biocontrol situations, through e.g., plant breeding for improved HIPV production, conditioning of mass-reared predators to appropriate cues, and employment of “push–pull-strategies” by using HIPVs.     

Methyl salicylate production in tomato affects biotic interactions

The role of methyl salicylate (MeSA) production was studied in indirect and direct defence responses of tomato (Solanum lycopersicum) to the spider mite Tetranychus urticae and the root‐invading fungus Fusarium oxysporum f. sp. lycopersici, respectively. To this end, we silenced the tomato gene encoding salicylic acid methyl transferase (SAMT). Silencing of SAMT led to a major reduction in SAMT expression and MeSA emission upon herbivory by spider mites, without affecting the induced emission of other volatiles (terpenoids). The predatory mite Phytoseiulus persimilis, which preys on T. urticae, could not discriminate between infested and non‐infested SAMT‐silenced lines, as it could for wild‐type tomato plants. Moreover, when given the choice between infested SAMT‐silenced and infested wild‐type plants, they preferred the latter. These findings are supportive of a major role for MeSA in this indirect defence response of tomato. SAMT‐silenced tomato plants were less susceptible to a virulent strain of F. oxysporum f. sp. lycopersici, indicating that the direct defense responses in the roots are also affected in these plants. Our studies show that the conversion of SA to MeSA can affect both direct and indirect plant defence responses.     

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

Summary Induction 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.     

Induced Response of Tomato Plants to Injury by Green and Red Strains of Tetranychus Urticae

We studied the induced response of tomato plants to the green strain and the red strain of the spider mite Tetranychus urticae. We focused on the olfactory response of the predatory mite Phytoseiulus persimilis to volatiles from T. urticae-infested tomato leaves in a Y-tube olfactometer. Tomato leaves attracted the predatory mites when slightly infested with the red strain, or moderately or heavily infested with the green strain. In contrast, neither leaves that were slightly infested with green-strain mites, nor leaves that were moderately or heavily infested with the red strain attracted the predators. We discuss the specific defensive responses of tomato plants to each of the two strains.     

Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae

In response to herbivory by insects, several plant species have been shown to produce volatiles that attract the natural enemies of those herbivores. Using a Y‐tube olfactometer, we investigated responses of the aphid parasitoid Diaeretiella rapae MacIntosh (Hymenoptera: Aphidiidae) to volatiles from Arabidopsis thaliana Columbia (Brassicaceae) plants that were either undamaged, infested by the peach‐potato aphid, Myzus persicae Sulzer (Homoptera: Aphididae), or mechanically damaged, as well as to volatiles from just the aphid or its honeydew. In dual‐choice experiments, female D. rapae given oviposition experience on A. thaliana infested with M. persicae were significantly attracted to volatiles from A. thaliana infested with M. persicae over volatiles from undamaged A. thaliana and similarly were significantly attracted to plants that had been previously infested by M. persicae, but from which the aphids were removed, over undamaged plants. Diaeretiella rapae did not respond to volatiles from M. persicae alone, their honeydew, or plants mechanically damaged with either a pin or scissors. We conclude that an interaction between the plant and the aphid induces A. thaliana to produce volatiles, which D. rapae can learn and respond to. Poor responses of D. rapae to volatiles from an A. thaliana plant that had two leaves infested with M. persicae, with the two infested leaves being removed before testing, suggested the possibility that, at this stage of infestation, the majority of volatile production induced by M. persicae may be localized to the infested tissues of the plant. We conclude that this tritrophic interaction is a suitable model system for future investigations of the biochemical pathways involved in the production of aphid‐induced volatiles attractive to natural enemies.     

Duration of Priming of Two Indirect Plant Defenses

When plants are infested by herbivores, they emit herbivore-induced plant volatiles (HIPVs) that attract carnivorous natural enemies of herbivores. Furthermore, there are increasing evidences that defenses of intact plants against herbivores are primed when exposed to HIPVs. We previously reported that lima bean leaf volatiles induced by the herbivorous mites Tetranychus urticae primed two T. urtiae-induced indirect defenses in neighboring conspecific plants: HIPV emission and extrafloral nectar (EFN) secretion. An intriguing unanswered question is whether the durations of these two defenses are the same. Here, we show that the durations of the two defenses were the same for up to two days after the initiation of T. urticae damage. The two induced primed defense would act as a battery of defense in exposed plants.Key Words: herbivore-induced plant volatiles, indirect, defense, induced response, plant-plant interaction, primingWhen infested by herbivores, plants defend themselves indirectly by emitting herbivore-induced plant volatiles (HIPVs). One of the ecological functions of HIPVs is to attract carnivorous natural enemies of the herbivores.^1,2 Recently, it was reported that the emission of HIPVs primed defenses against herbivores in neighboring intact plants.^3–7 Thus, HIPVs also mediate interactions between infested and intact plants.⁸ The enhanced defense in response to HIPVs in intact plants is called ‘priming’, which has been studied intensively in plant-pathogen interactions,⁹ but not so in plant-insect interactions.We previously reported that exposure to HIPVs emitted from lima bean leaves infested by Tetranychus urticae primed HIPV production in detached intact conspecific leaves.³ We also reported that exposure to HIPVs, produced in response to T. urticae damage,⁴ primed the induced production of extrafloral nectar (EFN; an alternative food source for predators^10,11 in lima bean plants. An intriguing question is whether the two primed defenses work as a battery against T. urticae. To answer this, we examined the duration of primed HIPV production by lima bean plants using the same experimental set-up as our previous study of EFN priming by conspecific plants.⁴For exposure of plants to HIPVs, we used a 60 × 60 × 60 cm cage with two 30 × 30 cm windows on opposite sides of the cage.¹² As odor sources, we used eight plants that had been infested with 60 adult T. urticae females per plant for 1 day. Eight uninfested plants were used as control odor sources. Two uninfested plants were placed in a cage with the odor source plants and exposed to either HIPVs or uninfested plant volatiles (UPVs) for 10 days in a climate-controlled room (25 ± 2°C, 60–70% RH, 16:8; L:D).A Y-tube olfactometer¹³ was used to examine the response of the predators to HIPVs. Adult female P. persimilis were randomly selected from a colony and individually positioned at the beginning of the iron wire. When test mites reached the end of one arm of the olfactometer, their choice was recorded. We tested the olfactory responses of the predator toward (1) plants infested by T. urticae for two days after exposure to UPVs vs. plants infested by T. urticae for two days after exposure to HIPVs, and (2) plants infested by T. urticae for four days after exposure to UPVs vs. plants infested by T. urticae for four days after exposure to HIPVs.HIPV-exposed plants attracted more predators than UPV-exposed plants in a Y-tube olfactometer when infested by T. urticae for two days (Fig. 1A). By contrast, the predators did not distinguish between HIPV- and UPV-exposed plants when infested by T. urticae for four days (Fig. 1B). Our previous study showed that HIPV-exposed plants secreted significantly larger amounts of EFN secretion than UPV-exposed plants infested by T. urticae for two days under the same experimental condition as in this study.⁴ However, the difference was not significant when they were infested for four days.⁴Open in a separate windowFigure 1The olfactory response of P. persimilis females to volatiles from the odor-exposed plants, as determined in a Y-tube olfactometer: (A) plants infested by T. urticae for two days after exposure to UPVs (UPV-exposed—T. urticae 2d) vs. plants infested by T. urticae for two days after exposure to HIPVs (HIPV-exposed—T. urticae 2d), and (B) plants infested by T. urticae for four days after exposure to UPVs (UPV-exposed—T. urticae 4d) vs. plants infested by T. urticae for four days after the exposure to HIPVs (HIPV-exposed—T. urticae 4d). Asterisks beside each bar indicate a significant difference between the first trifoliate leaves and the primary leaves. Asterisks beside a bar indicate a significant difference (binomial test: p < 0.001).Lima bean plants increase the amount of endogenous jasmonic acid after exposure to HIPVs.¹⁴ Jasmonic acid, an important plant hormone regulating a defense signaling pathway against herbivores and pathogens,^15,16 is reported to be involved in the induction of both volatile emission^17,18 and EFN secretion¹⁹ in response to T. urticae damage in lima bean plants. The increase of endogenous jasmonic acid in HIPV-exposed plants may partly explain the simultaneous priming of the two defenses.In this study, we showed that the durations of priming of two indirect defenses were roughly the same for up to two days. Priming of these two indirect defenses would thus be a battery of defense at the outset of T. urticae damage. Further study is necessarily to test whether the primed battery of induced defense increases the fitness of the exposed plants.     

Effects of quantitative and qualitative differences in volatiles from host‐ and non‐host‐infested maize on the attraction of the larval parasitoid Cotesia kariyai

Cotesia kariyai Watanabe (Hymenoptera: Braconidae) is a specialist larval parasitoid of Mythimna separata Walker (Lepidoptera: Noctuidae). Cotesia kariyai wasps use herbivore‐induced plant volatiles (HIPVs) to locate hosts. However, complex natural habitats are full of volatiles released by both herbivorous host‐ and non‐host‐infested plants at various levels of intensity. Therefore, the presence of non‐hosts may affect parasitoid decisions while foraging. Here, the host‐finding efficiency of naive C. kariyai from HIPVs influenced by host‐ and non‐host‐infested maize [Zea mays L. (Poaceae)] plants was investigated with a four‐arm olfactometer. Ostrinia furnacalis Guenée (Lepidoptera: Crambidae) was selected as a non‐host species. One unit (1 U) of host‐ or non‐host‐infested plant was prepared by infesting a potted plant with five host or seven non‐host larvae. In two‐choice bioassays, host‐infested plants fed upon by different numbers of larvae, and various units of host‐ and non‐host‐infested plants (infestation units; 1 U, 2 U, and 3 U) were arranged to examine the effects of differences in volatile quantity and quality on the olfactory responses of C. kariyai with the assumption that volatile quantity and quality changes with differences in numbers of insects and plants. Cotesia kariyai was found to perceive quantitative differences in volatiles from host‐infested plants, preferring larger quantities of volatiles from larger numbers of larvae or plants. Also, the parasitoids discriminated between healthy plants, host‐infested plants, and non‐host‐infested plants by recognising volatiles released from those plants. Cotesia kariyai showed a reduced preference for host‐induced volatiles, when larger numbers of non‐host‐infested plants were present. Therefore, quantitative and qualitative differences in volatiles from host‐ and non‐host‐infested plants appear to affect the decision of C. kariyai during host‐habitat searching in multiple tritrophic systems.     

Preference of Neoseiulus californicus (Acari: Phytoseiidae) for volatiles of Bt maize induced by multiple herbivory

Plant indirect induced defenses against herbivores are characterized by the production of plant volatiles that to attract natural enemies. The objective of this study was to evaluate whether the attack of the two-spotted spider mite Tetranychus urticae or the multiple herbivory of T. urticae together with the fall armyworm Spodoptera frugiperda are able to elicit indirect induced defense in conventional and Bt maize plants. The experiment was carried out in the laboratory using Y-tube olfactometer, evaluating the predatory mite Neoseiulus californicus olfactory preference for plant volatiles. The treatments involved: Clean Conventional Plant; Conventional Plant Infested with T. urticae; Clean Bt Plant; Bt Plant Infested with T. urticae; Conventional Plant Infested with T. urticae + fall armyworm; Bt Plant Infested with T. urticae + fall armyworm. For the chemical analyzes the Trace GC Ultra gas chromatograph was used, paired with the Polaris Q mass spectrometer, GCMS system. Neoseiulus californicus was also unable to distinguish between volatiles from both conventional and Bt infested maize plants. Moreover, there was no discrimination of the predator mite between plants under single and multiple infestations, both in conventional and Bt maize. When comparing conventional and Bt plants, both with multiple infestation, the predator mite N. californicus had no preference among these sources of odors. However, there was observed chemical changes of the volatiles among the groups of plants studied. Thus, it is suggested that the groups of plants under study have chemical modifications, but they are not able to attract N. californicus. In addition, Bt plants response was similar to conventional plants on attracting N. californicus.     

Non‐pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid‐induced plant volatiles via jasmonic acid signalling

Beneficial soil‐borne microbes, such as mycorrhizal fungi or rhizobacteria, can affect the interactions of plants with aboveground insects at several trophic levels. While the mechanisms of interactions with herbivorous insects, that is, the second trophic level, are starting to be understood, it remains unknown how plants mediate the interactions between soil microbes and carnivorous insects, that is, the third trophic level. Using Arabidopsis thaliana Col‐0 and the aphid Myzus persicae, we evaluate here the underlying mechanisms involved in the plant‐mediated interaction between the non‐pathogenic rhizobacterium Pseudomonas fluorescens and the parasitoid Diaeretiella rapae, by combining ecological, chemical and molecular approaches. Rhizobacterial colonization modifies the composition of the blend of herbivore‐induced plant volatiles. The volatile blend from rhizobacteria‐treated aphid‐infested plants is less attractive to an aphid parasitoid, in terms of both olfactory preference behaviour and oviposition, than the volatile blend from aphid‐infested plants without rhizobacteria. Importantly, the effect of rhizobacteria on both the emission of herbivore‐induced volatiles and parasitoid response to aphid‐infested plants is lost in an Arabidopsis mutant (aos/dde2‐2) that is impaired in jasmonic acid production. By modifying the blend of herbivore‐induced plant volatiles that depend on the jasmonic acid‐signalling pathway, root‐colonizing microbes interfere with the attraction of parasitoids of leaf herbivores.     

The influence of host plant species on parasitism of pollen beetles (Meligethes spp.) by Phradis morionellus

We investigated the response of the specialist insect predator Oligota kashmirica benefica (Coleoptera: Staphylinidae) to volatiles from lima bean leaves infested with the spider mite Tetranychus urticae (Acari: Tetranychidae), both in a Y-tube olfactometer and in a field in Kyoto, Japan. Adult male and female predators were significantly more attracted to T. urticae-infested leaves than to clean air. Adult male and female predators were not more attracted to uninfested leaves, artificially damaged leaves, or the spider mites and their visible products when compared to clean air. In a field trap experiment, 12 adult predators were caught in three traps containing T. urticae-infested lima bean plants over 13 days, whereas no adult predators were trapped in three traps containing uninfested lima bean plants during the same period. These results showed that O. kashmirica benefica adults responded to herbivore-induced plant volatiles from T. urticae-infested lima bean leaves under both laboratory and field conditions.     

Similar attractiveness of maize volatiles induced by Helicoverpa armigera and Pseudaletia separata to the generalist parasitoid Campoletis chlorideae

Campoletis chlorideae Uchida (Hymenoptera: Ichneumonidae), a major larval endoparasitoid of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), also attacks many other noctuid caterpillars. We investigated the attractiveness of H. armigera‐ and Pseudaletia separata (Lepidoptera: Noctuidae)‐infested maize [Zea mays L. (Poaceae)] plants to C. chlorideae, and analyzed the volatiles emitted from infested plants and undamaged plants. Considering the reported specific induction of plant volatiles by elicitors in the caterpillar regurgitant, we also tested the response of the parasitoid to mechanically damaged plants treated with caterpillar regurgitant or water and measured the volatiles released by these plants. In wind‐tunnel bioassays, C. chlorideae was strongly attracted to herbivore‐induced maize volatiles. Mechanically damaged plants, whether they were treated with caterpillar regurgitant or water, were more attractive to the parasitoid than undamaged plants. The parasitoid did not distinguish between maize seedlings infested by the two noctuid insects, nor did they show a difference in attraction to mechanically damaged plants treated with caterpillar regurgitant or water. Coupled gas chromatography–mass spectrometer (GC‐MS) analysis revealed that 15 compounds were commonly emitted by herbivore‐infested and mechanically damaged maize plants, whereas only two compounds were released in minor amounts from undamaged plants. Infestation by H. armigera specifically induced four terpenoids, β‐pinene, β‐myrcene, D‐limonene, and (E)‐nerolidol, which were not induced by infestation of P. separata and mechanical damage, plus caterpillar regurgitant or water. Two compounds, geranyl acetate and β‐sesquiphellandrene, were also induced by the infestation of H. armigera, but not by the infestation of P. separata. All treated maize plants released volatiles in significantly larger total amounts than did undamaged plants. Maize plants infested by H. armigera emitted greater amounts of volatiles than plants infested by P. separata. The treatment with caterpillar regurgitant resulted in larger amounts of volatile emission than the treatment with water did in mechanically damaged plants. The amounts of emissions of individual compounds were also different between differently treated plants.     

Variation in the olfactory response of 13 populations of the predatory mite Amblyseius womersleyi to Tetranychus urticae-infested plant volatiles (Acari: Phytoseiidae, Tetranychidae)

We studied the response of the predatory mite Amblyseius womersleyi collected in 13 different sites in Japan toward Tetranychus urticae-infested kidney bean leaf volatiles in a Y-tube olfactometer. The predatory mites were collected from eight plant species infested by one of three tetranychid mite species. The predators' responses to the infested-leaf volatiles varied from 33% to 97% among the populations. The predators collected at 10 sites showed a significant preference for infested-leaf volatiles, whereas those collected at three tea plantations did not distinguish between the infested- and uninfested-leaf volatiles. We discussed the possible factors that affected the olfactory response of A. womersleyi towards the infested leaf volatiles.     

The distribution of herbivores between leaves matches their performance only in the absence of competitors

Few studies have tested how plant quality and the presence of competitors interact in determining how herbivores choose between different leaves within a plant. We investigated this in two herbivorous spider mites sharing tomato plants: Tetranychus urticae, which generally induces plant defenses, and Tetranychus evansi, which suppresses them, creating asymmetrical effects on coinfesting competitors. On uninfested plants, both herbivore species preferred young leaves, coinciding with increased mite performance. On plants with heterospecifics, the mites did not prefer leaves on which they had a better performance. In particular, T. urticae avoided leaves infested with T. evansi, which is in agreement with T. urticae being outcompeted by T. evansi. In contrast, T. evansi did not avoid leaves with the other species, but distributed itself evenly over plants infested with heterospecifics. We hypothesize that this behavior of T. evansi may prevent further spread of T. urticae over the shared plant. Our results indicate that leaf age determines within‐plant distribution of herbivores only in absence of competitors. Moreover, they show that this distribution depends on the order of arrival of competitors and on their effects on each other, with herbivores showing differences in behavior within the plant as a possible response to the outcome of those interactions.     

Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites

We found that intact lima bean plants increased the secretion of extrafloral nectar (EFN) after exposure to Tetranychus urticae-induced plant volatiles. Predatory mites, Phytoseiulus persimilis, dispersed more slowly from an exposed intact plant than from a control plant (plant exposed to volatiles from intact conspecific). The predators also dispersed more slowly from those plants that were provided with extra EFN than from untreated plants. We further show that EFN was a potential alternative food source for P. persimilis. From these results, we concluded that increased EFN was involved in the slow dispersal of P. persimilis from the plants exposed to herbivore-induced plant volatiles. Our data suggest that the increase of EFN in an HIPV-exposed intact plant could be an induced indirect defense against spider mites.     

Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores

It is well known that herbivore-induced plant defenses alter host plant quality and can affect the behavior and performance of later arriving herbivores.Effects of sequential attacks by herbivores that either suppress or induce plant defenses are less well studied.We sequentially infested leaves of tomato plants with a strain of the phytophagous spider mite Tetranychus urticae that induces plant defenses and the closely related Tetranychus evansi, which suppresses plant defenses.Plant quality was quantified through oviposifion of both spider mite species and by measuring proteinase inhibitor activity using plant material that had been sequentially attacked by both herbivore species.Spider-mite oviposifion data show that T.evansi could suppress an earlier induction of plant defenses by T.urticae,and T.urticae could induce defenses in plants previously attacked by T.evansi in 1 day.Longer attacks by the second species did not result in further changes in oviposifion.Proteinase inhibitor activity levels showed that T.evansi suppressed the high activity levels induced by T.urticae to constitutive levels in 1 day,and further suppressed activity to levels similar to those in plants attacked by T.evansi alone.Attacks by T.urticae induced proteinase inhibitor activity in plants previously attacked by T.evansi,eventually to similar levels as induced by T.urticae alone.Hence,plant quality and plant defenses were significantly affected by sequential attacks and the order of attack does not affect subsequent performance,but does affect proteinase inhibitor activity levels.Based on our results,we discuss the evolution of suppression of plant defenses.     

Local and distant prey-related cues influence when an acarine predator leaves a prey patch

Over relatively long distances, the predatory mite Phytoseiulus persimilis is able to detect volatiles produced by bean plants that are infested by its prey, Tetranychus urticae, the twospotted spider mite. Our investigation examined the separate and combined effects of prey, their products, and prey-induced plant volatiles on when P. persimilis left a potential prey host plant. In wind tunnels, we assessed the relative importance of and interaction among local and distant prey-related cues. The examination of local cues included: (1) all local cues (prey eggs, webbing, and prey-induced plant volatiles), (2) food (prey eggs) and webbing only, (3) plant volatiles only, and (4) no prey-related cues. The examination of distant cues involved the presence or absence of prey-induced plant volatiles from upwind plants. External volatile cues, produced by placing prey-infested plants upwind in the wind tunnel, resulted in more predators leaving downwind plants, and leaving sooner, than when clean plants were upwind, regardless of the availability of prey or prey-related cues on the local plant. However, local cues, especially the presence of food/webbing, had a greater effect than distant cues on timing of predator leaving. Predators remained in larger numbers and for longer times on prey-infested plants. However, the presence of either locally-produced plant volatiles or food/webbing alone still reduced the number of predators leaving a plant in the first hour compared to clean plants. After the first hour, the number of predators leaving was primarily driven by the presence of food/webbing. When no food/webbing was available, predators left plants rapidly; if food/webbing was available, some predatory mites remained on plants at least 24 hours. Even if no food/webbing was available, predators presented with local volatiles remained on plants for several hours longer than on clean plants without local volatiles. These small changes in leaving rates may lead to differences in local population dynamics, and possibly regional persistence, of the predator-prey interaction in patchy environments.     

Application of synthetic herbivore‐induced plant volatiles causes increased parasitism of herbivores in the field

We previously reported that Cotesia vestalis (Hymenoptera, Braconidae), a parasitoid of diamondback moth (DBM) (Plutella xylostella; Lepidoptera, Plutellidae) larvae, was attracted to volatiles from crucifer plants infested by moth larvae kept in a desktop acrylic box, and that a blend of four DBM‐induced plant volatiles was responsible for this attraction. In this study, using a specially designed dispenser to release the four compounds, we demonstrated that the wasp was attracted to intact komatsuna plants (Brassica rapa var. perviridis). The experiments were performed in a climate‐controlled room, which was approximately 1000 times larger than the acrylic box used previously. Similarly, using the dispenser in the field, C. vestalis females were attracted to intact komatsuna plants with the dispenser from a distance of three metres. We also examined the effect of the volatile blend on the incidence of parasitism of DBM larvae in the field. Three small containers containing DBM‐infested komatsuna plants with dispensers, and three control containers containing only infested plants (control) were arranged in two lines running perpendicular to a komatsuna field in which both DBM larvae and C. vestalis populations were maintained, at distances of 12, 30 and 70 m. The results showed that the incidence of DBM parasitism was significantly higher in containers containing dispensers than in the control containers, suggesting that the blend could potentially be applied to DBM control in agroecosystems.