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.     

Attraction of a generalist predator towards herbivore-infested plants

The occurrence and strength of interactions among natural enemies and herbivores depend on their foraging decisions, and several of these decisions are based on odours. To investigate interactions among arthropods in a greenhouse cropping system, we studied the behavioural response of the predatory bug Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) towards cucumber plants infested either with thrips (Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)) or with spider mites (Tetranychus urticae Koch (Acari: Tetranychidae)). In greenhouse release-recapture experiments, the predatory bug showed a significant preference for both thrips-infested plants and spider mite-infested plants over clean plants. Predatory bugs preferred plants infested with spider mites to plants with thrips. Experience with spider mites on cucumber leaves prior to their release in the greenhouse had no effect on the preference of the predatory bugs. However, this experience did increase the percentage of predators recaptured. Y-tube olfactometer experiments showed that O. laevigatus was more attracted to odours from plants infested with spider mites than to odours from clean plants. Thus, O. laevigatus is able to perceive odours and may use them to find plants with prey in more natural conditions. The consequences of the searching behaviour for pest control are discussed.     

Males of the predatory mirid bug Macrolophus caliginosus exploit plant volatiles induced by conspecifics as a sexual synomone

The olfactory responses of male and female Macrolophus caliginosus Wagner (Heteroptera: Miridae) adults towards volatiles from green bean plants previously exposed to feeding by conspecifics and to direct odours from conspecifics were tested in a Y-tube olfactometer. Female M. caliginosus did not respond to volatiles from plants exposed to mirid feeding or to odours emitted directly by adult mirids. In contrast, male mirid bugs were attracted both to volatiles from plants previously exposed to feeding by conspecific females and to odours emitted by conspecifics only with a marginally significant preference for the former. The gas chromatography-mass spectrometry analysis showed that mirid feeding induced the release of 11 additional compounds as compared to the volatiles emitted from clean plants. Three of these substances (5-ethyl-2(5H)-furanone, Z-3-hexenyl tiglate, and E,E-α-farnesene) were released only after feeding by females. Furthermore, 21 compounds were identified in volatiles emitted directly by mirids, 12 of which were unique to the mirids (i.e., not present in clean plants or plants previously exposed to mirid feeding). The results suggest that female-specific herbivore-induced plant volatiles play a role as mate-finding cues by the male mirids. The ecological implications of the findings are discussed, and the term ‘sexual synomone’ is introduced.     

Macrolophus caliginosus: Functional response to whiteflies and preference and switching capacity between whiteflies and spider mites

Laboratory experiments were performed with adult female Macrolophus caliginosus Wagner (Heteroptera: Miridae) at 22ºC on bean plants to determine the functional response towards whiteflies, as well as the preference and switching capacity between the two prey species: whiteflies and spider mites. Predation of females presented with first instars of Trialeurodes vaporariorum Westwood (Homoptera: Aleyrodidae) was of a Type III functional response. The observed maximum predation was approximately 75 first instars at high prey densities within a 24-h period. The preference of M. caliginosus females between eggs of T. vaporariorum and Tetranychus urticaeKoch (Acarina: Tetranychidae) changed with the ratio of offered prey. The preference for T. vaporariorum eggs increased non-linearly with increasing proportions of this prey type. The average maximum predation of whitefly and spider mite eggs were approximately 166 and 111 eggs per day, respectively, at the highest ratio of the two preys. The proportion of M. caliginosus females found on the test plants at the end of the experiment increased with prey density suggesting that this mirid spends more time in areas with high prey density. Macrolophus caliginosus females are voracious predators of eggs and first instars of T. vaporariorum as well as of spider mite eggs and may thus be a valuable addition to existing methods of biological control of T. vaporariorum and T. urticae.     

Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors

Plants under herbivore attack produce volatiles, thus attracting natural enemies of the herbivores. However, in doing so, the plant becomes more conspicuous to other herbivores. Herbivores may use the odours as a cue to refrain from visiting plants that are already infested, thereby avoiding competition for food, or, alternatively, to visit plants with defences weakened by earlier attacks. We investigated the response of one species of herbivore (the spider mite Tetranychus urticae) to odours emanating from cucumber plants infested by conspecific or heterospecific (the western flower thrips, Frankliniella occidentalis) herbivores. Olfactometer experiments in the laboratory showed that spider mites have a slight, but significant, preference for plants infested with conspecifics, but strongly avoid plants with thrips. These results were substantiated with greenhouse experiments. We released spider mites on the soil in the centre of a circle of six plants, half of which were infested with either conspecifics or heterospecifics (thrips), whereas the other half were uninfested. It was found that 60–70% of the mites were recaptured on the plants within 5 h after release. Results of these experiments were in agreement with results of the olfactometer experiments: (1) significantly fewer spider mites were found on plants infested with thrips than on uninfested plants and (2) more mites were found on plants with conspecifics than on clean plants (although this difference was not significant). From a functional point of view it makes sense that spider mites prefer clean plants over thrips-infested plants, since thrips are not only competitors, but are also known as intraguild predators of spider mites. Possible reasons for the slight attraction of spider mites to plants infested with conspecifics are discussed. Received: 22 June 1996 / Accepted: 29 September 1996     

Interactions in a tritrophic acarine predator-prey metapopulation system V: Within-plant dynamics of Phytoseiulus persimilis and Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae)

To investigate the relative contributions of bottom-up (plant condition) and top-down (predatory mites) factors on the dynamics of the two-spotted spider mite (Tetranychus urticae), a series of experiments were conducted in which spider mites and predatory mites were released on bean plants. Plants inoculated with 2, 4, 8, 16, and 32 adult female T. urticae were either left untreated or were inoculated with 3 or 5 adult female predators (Phytoseiulus persimilis) one week after the introduction of spider mites. Plant area, densities of T. urticae and P. persimilis, and plant injury were assessed by weekly sampling. Data were analysed by a combination of statistical methods and a tri-trophic mechanistic simulation model partly parameterised from the current experiments and partly from previous data. The results showed a clear effect of predators on the density of spider mites and on the plant injury they cause. Plant injury increased with the initial number of spider mites and decreased with the initial number of predators. Extinction of T. urticae, followed by extinction of P. persimilis, was the most likely outcome for most initial combinations of prey and predators. Eggs constituted a relatively smaller part of the prey population as plant injury increased and of the predator population as prey density decreased. We did not find statistical evidence of P. persimilis having preference for feeding on T. urticae eggs. The simulation model demonstrated that bottom-up and top-down factors interact synergistically to reduce the density of spider mites. This may have important implications for biological control of spider mites by means of predatory mites.     

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.     

Evaluation of the predatory mite <Emphasis Type="Italic">Phytoseiulus macropilis</Emphasis> (Acari: Phytoseiidae) as a biological control agent of the two-spotted spider mite on strawberry plants under greenhouse conditions

The predatory mite Phytoseiulus macropilis is a potential biological control agent of the two-spotted spider mite (TSSM) Tetranychus urticae on strawberry plants. Its ability to control TSSM was recently assessed under laboratory conditions, but its ability to locate and control TSSM under greenhouse conditions has not been tested so far. We evaluated whether P. macropilis is able to control TSSM on strawberry plants and to locate strawberry plants infested with TSSM under greenhouse conditions. Additionally, we tested, in an olfactometer, whether odours play a role in prey-finding by P. macropilis. The predatory mite P. macropilis required about 20 days to achive reduction of the TSSM population on strawberry plants initially infested with 100 TSSM females per plant. TSSM-infested plants attract an average of 27.5 ± 1.0% of the predators recaptured per plant and uninfested plants attracted only 5.8 ± 1.0% per plant. The predatory mites were able to suppress TSSM populations on a single strawberry plant and were able to use odours from TSSM-infested strawberry plants to locate prey in both olfactometer and arena experiments. Hence, it is concluded that P. macropilis can locate and reduce TSSM population on strawberry plants under greenhouse conditions.     

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.     

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.     

Response of predatory mites with different rearing histories to volatiles of uninfested plants

The behavioural response of the predatory mite Phytoseiulus persimilis to volatiles from several host plants of its prey, spider mites in the genus Tetranychus, was investigated in a Y-tube olfactometer. A positive response to volatiles from tomato leaves and Lima bean leaves was recorded, whereas no response was observed to volatiles from cucumber leaves, or leaves of Solanum luteum and Solanum dulcamara.Different results were obtained for predators that differed in rearing history. Predators that were reared on spider mites (Tetranychus urticae) on Lima bean leaves did respond to volatiles from Lima bean leaves, while predators that had been reared on the same spider mite species but with cucumber as host plant did not respond to Lima bean leaf volatiles. This effect is compared with the effect of rearing history on the response of P. persimilis to volatile allelochemicals of prey-infested plant leaves.     

Do spider mite-infested plants and spider mite trails attract predatory mites?

We questioned the well-accepted concept that spider mite-infested plants attract predatory mites from a distance. This idea is based on the preference demonstrated by predatory mites such as Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) for volatiles produced by spider mite-infested plants in a closed environment (Y-tube wind tunnel). However, in natural open environments, kidney bean leaves heavily infested with Tetranychus urticae Koch (Acari: Tetranychidae) did not attract P. persimilis from the same distances as were used in the Y-tube tests. Therefore, the attraction of predatory mites for spider mite-infested plant volatiles in the Y-tube tests may reflect a preference in a closed environment and should be carefully interpreted as a basis for extrapolating predator–prey attraction mechanisms in the wild. On the other hand, we showed that adult female P. persimilis could follow trails laid down by adult female T. urticae in the laboratory and in natural open environments. Consequently, we propose that following spider mite trails represents another prey-searching cue for predatory mites.     

Genetic variations in a population of herbivorous mites Tetranychus urticae in the production of the induced volatiles by kidney bean plants

Abstract

This study tested whether a population of herbivorous mites Tetranychus urticae exhibits genetic variation in the production of induced plant volatiles in kidney bean plants (Phaseolus vulgaris L.). We selected two T. urticae genotypes based on their dispersal behavior (early- and late-disperser) in two plant lines (Line-1 and Line-2). In both lines, plants infested by the early-disperser produced large amounts of induced volatiles after the spider mite population peaked on the plants, whereas those infested by the late-disperser emitted the largest amount of induced volatiles at the population peak. The possible manipulation of the production of herbivore-induced plant volatiles by herbivores is discussed.     

A key volatile infochemical that elicits a strong olfactory response of the predatory mite <Emphasis Type="Italic">Neoseiulus californicus</Emphasis>, an important natural enemy of the two-spotted spider mite <Emphasis Type="Italic">Tetranychus urticae</Emphasis>

Herbivore-induced plant volatiles (HIPVs) emitted from lima bean leaves infested with the two-spotted spider mites Tetranychus urticae strongly attract the predatory mites Neoseiulus californicus. Among these HIPVs, methyl salicylate and linalool can attract the predators. Three green-leaf volatiles (GLVs) of (Z)-3-hexen-1-ol, (Z)-3-hexenyl acetate and (E)-2-hexenal, found in the odor blends from T. urticae-infested leaves and physically damaged leaves, can also attract the predators. To search for a strong predator attractant, the olfactory responses of N. californicus to each synthetic compound or their combinations were investigated in a Y-tube olfactometer. When presented a choice between a mixture of the five compounds (i.e. the two HIPVs and the three GLVs) and T. urticae-infested leaves, N. californicus did not discriminate between these odor sources. The same trend was observed when either a mixture of the two HIPVs or methyl salicylate vs. T. urticae-infested leaves were compared. In contrast, the predators preferred T. urticae-infested leaves to linalool, each of the three GLVs, or a mixture of the three GLVs. These results indicated that methyl salicylate is a strong predator attractant, and its potential attractiveness almost equaled that of the blend of HIPVs from T. urticae-infested leaves.     

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.     

Migration of specialist insect predators to exploit patchily distributed spider mites

It is believed that specialist predators of spider mites often migrate by flight or aerial transport to exploit patchily distributed prey. The migration is an important factor in determining the seasonal occurrence of the predators in a field. Several species of specialist insect predators, such as Oligota kashmirica benefica (Coleoptera: Staphylinidae) and Scolothrips takahashii (Thysanoptera: Thripidae), migrate between orchard trees and plants near the trees (e.g., groundcover, weeds, or windbreaks) to exploit abundant spider mites. This migration is at least partly triggered by prey scarcity in the original local habitats. Although these predators are tiny insects, they have flight abilities. For example, adult O. kashmirica benefica (body length, ∼1 mm) could move at least 5–16 m in one flight. Presumably, migration of the insect predators between prey-infested plants occurs mainly by flights. Predatory mites, such as Amblyseius fallacis and Amblyseius womersleyi (Acari: Phytoseiidae), migrated to spider mite-infested plants outside an orchard by aerial transport when they suffered from prey scarcity in the orchard. S. takahashii can use plant volatiles from lima bean plants induced by the spider mite Tetranychus urticae as cues for prey location during migration in Satsuma mandarin groves. However, it remains unknown how far from the trap boxes S. takahashii could respond to herbivore-induced plant volatiles in the groves. Received: August 25, 2000 / Accepted: February 1, 2001     

Do Herbivore-Induced Plant Volatiles Influence Predator Migration and Local Dynamics of Herbivorous and Predatory Mites?

If predators lack information on the prey's position, prey have more chance to escape predation and will therefore reach higher population densities. One of the many possible cues that predators may use to find their prey are herbivore-induced plant volatiles. Although their effects on the behaviour of foraging predators have been well studied, little is known about how these prey-related odours affect predator–prey dynamics on a plant. We hypothesise that herbivore-induced plant volatiles provide the major cue eliciting predator arrestment on prey-infested leaves and that the response to these volatiles ultimately leads to lower prey densities. To test this hypothesis experimentally, we created two types of odour-saturated environments: one with herbivore-induced plant volatiles (treatment), and one with green-leaf volatiles (control). An odour-free environment could not be tested because herbivores require plants for population growth. We measured the rate at which predatory mites (Phytoseiulus persimilis) immigrate, emigrate and exploit a single leaf infested by two-spotted spider mites (Tetranychus urticae). The experiments did not show a significant difference between treatment and control. At best, there was a somewhat higher rate of predator (and possibly also prey) emigration in the treatment. The lack of a pronounced difference between treatment and control indicates that at the spatial scale of the experiments random searching for prey was as effective as directional searching. Alternatively, predators were arrested in the prey patch by responding not merely to herbivore-induced plant volatiles, but also to other prey-related cues, such as web and faeces. Based on our current experience we advocate to increase the spatial scale of the experiment (>1m²) and we provide other suggestions for improving the set-up.     

Plant–plant–plant communications,mediated by (E)-β-ocimene emitted from transgenic tobacco plants,prime indirect defense responses of lima beans

Some volatile organic chemicals (VOCs), such as terpenes, are responsible for communication between plants. We assessed the priming of defense responses in lima bean by exposing the plants to transgenic-plant-volatiles [(E)-β-ocimene] emitted from transgenic tobacco plants (NtOS2). As it was previously shown that the first receiver lima bean plants, which were infested with spider mites after having been exposed to (E)-β-ocimene from NtOS2, were highly induced to emit VOCs, we analyzed the VOCs emitted from a second set of receiver plants (second receiver plants) exposed to the infested, first receiver plants. In response to feeding by spider mites, two homoterpenes [(E)-4,8-dimethyl-1,3,7-nonatriene and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene] were more highly emitted from the second receiver plants in response to spider mite attack, in comparison to the levels emitted from plants that had been placed near infested, wild-type (WT)-volatile-exposed plants. These data suggest that transgenic-plant-volatile-mediated, multiple-plant communication can function in plant defenses.     

Lotus japonicus Infested with Herbivorous Mites Emits Volatile Compounds That Attract Predatory Mites

Lotus Japonicus has an indirect defense mechanism against spider mites, Tetranychus urticae, we investigated the responses of predatory mites, Phytoseiulus persimilis, to volatile compounds released from T. urticae-infested L. japonicus in a Y-tube olfactometer. Plants infested with spider mites attracted more P. persimilis than did clean air. Uninfested plants and artificially damaged plants did not attract P. persimilis. When infested by spider mites, L. japonicus plants started emitting (Z)-3-hexenyl acetate, (E)-4,8-dimethyl-1,3,7-nonatriene, germacrene d, 1-octen-3-ol and methyl salicylate (MeSA). These compounds were considered to be T. urticae-induced plant volatile compounds. When three L. japonicus mutants deficient in nodule organogenesis were infested by the spider mites, they all attracted P. persimilis. However, two of the infested mutants emitted blends of induced volatile compounds that were qualitatively different from those emitted from infested wild type L. japonicus. Received 8 August 2000/ Accepted in revised form 12 October 2000     

Altered host plant preference of Tetranychus urticae and prey preference of its predator Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae) on transgenic Cry3Bb-eggplants

The behavior of the two-spotted spider mite, Tetranychus urticae Koch and the predatory mite Phytoseiulus persimilis A.-H. was investigated in laboratory experiments with transgenic Bt-eggplants, Solanum melongena L., producing the Cry3Bb toxin and corresponding isogenic, non-transformed eggplants. In bitrophic experiments, dual-choice disc tests were conducted to reveal the effects of transgenic eggplants on host plant preference of T. urticae. Adult spider mite females were individually placed on leaf discs (2 cm diameter) and were observed during five days. Females occurred significantly more frequently on transgenic halves on which also significantly more T. urticae eggs were found. The effects of a Cry3Bb-eggplant fed prey on the feeding preference of P. persimilis were investigated in tritrophic experiments. Sixteen spider mite females, eight of which had been taken from transgenic and eight from isogenic eggplants, were offered to well-fed females of P. persimilis and numbers of respective spider mites consumed were registered 12 h later when the predators were offered new spider mites again. This procedure was repeated six times. The results revealed that predatory mites consumed significantly less Bt-fed spider mites than prey that had been raised on control eggplants. These results indicate that eggplants expressing the Cry3Bb toxin for resistance against the Colorado potato beetle are more preferred by spider mites but are less preferred by their predator P. persimilis. Possible consequences of these findings for biological control of spider mites on eggplants are discussed.