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.     

Olfactory response of Typhlodromus pyri (Acari: Phytoseiidae) to synthetic methyl salicylate in laboratory bioassays

The herbivore‐induced plant volatile (HIPV) methyl salicylate (MeSA) is widely present in the chemical profile of several plant species and is known to attract natural enemies, including predatory mites. In this study, the response of Typhlodromus pyri, a key predator of pest mites in west coast vineyards, to synthetically produced MeSA was tested using a Y‐tube olfactometer in laboratory bioassays. Six doses ranging from 0.002 to 200 μg of MeSA diluted in 0.1 ml hexane were tested. Significantly higher proportions of T. pyri preferred MeSA at doses 0.02, 0.2 and 20 μg. No differences in response to MeSA were detected at the highest (200 μg), intermediate (2 μg) and lowest (0.002 μg) doses. Mite response to MeSA was a function of dose when fitting polynomial and logistic regression models using dose and square of the log dose prediction factors. Results indicate that synthetic MeSA may be applied to attract predatory arthropod populations in vineyards to enhance biological control of pest mites.     

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.     

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.     

Complex Odor from Plants under Attack: Herbivore's Enemies React to the Whole, Not Its Parts

Background

Insect herbivory induces plant odors that attract herbivores'' natural enemies. Assuming this attraction emerges from individual compounds, genetic control over odor emission of crops may provide a rationale for manipulating the distribution of predators used for pest control. However, studies on odor perception in vertebrates and invertebrates suggest that olfactory information processing of mixtures results in odor percepts that are a synthetic whole and not a set of components that could function as recognizable individual attractants. Here, we ask if predators respond to herbivore-induced attractants in odor mixtures or to odor mixture as a whole.

Methodology/Principal Findings

We studied a system consisting of Lima bean, the herbivorous mite Tetranychus urticae and the predatory mite Phytoseiulus persimilis. We found that four herbivore-induced bean volatiles are not attractive in pure form while a fifth, methyl salicylate (MeSA), is. Several reduced mixtures deficient in one component compared to the full spider-mite induced blend were not attractive despite the presence of MeSA indicating that the predators cannot detect this component in these odor mixtures. A mixture of all five HIPV is most attractive, when offered together with the non-induced odor of Lima bean. Odors that elicit no response in their pure form were essential components of the attractive mixture.

Conclusions/Significance

We conclude that the predatory mites perceive odors as a synthetic whole and that the hypothesis that predatory mites recognize attractive HIPV in odor mixtures is unsupported.     

Attraction of Phytoseiulus persimilis (Acari: Phytoseiidae) towards volatiles from various Tetranychus urticae-infested plant species

Plants infested with the spider mite Tetranychus urticae Koch, may indirectly defend themselves by releasing volatiles that attract the predatory mite Phytoseiulus persimilis Athias-Henriot. Several plants from different plant families that varied in the level of spider mite acceptance were tested in an olfactometer. The predatory mites were significantly attracted to the spider mite-infested leaves of all test plant species. No differences in attractiveness of the infested plant leaves were found for predatory mites reared on spider mites on the different test plants or on lima bean. Thus, experience with the spider mite-induced plant volatiles did not affect the predatory mites. Jasmonic acid was applied to ginkgo leaves to induce a mimic of a spider mite-induced volatile blend, because the spider mites did not survive when incubated on ginkgo. The volatile blend induced in ginkgo by jasmonic acid was slightly attractive to predatory mites. Plants with a high degree of direct defence were thought to invest less in indirect defence than plants with a low degree of direct defence. However, plants that had a strong direct defence such as ginkgo and sweet pepper, did emit induced volatiles that attracted the predatory mite. This indicates that a combination of direct and indirect defence is to some extent compatible in plant species.     

Evolutionary adaptation to host plants in a laboratory population of the phytophagous mite Tetranychus urticae Koch

Summary For evolutionary expansion of host range to occur in an herbivore population, genetic variation in ability to survive on and/or accept new hosts must be present. To determine whether a population of the phytophagous mite Tetranychus urticae contained such variation, I established lines from the population on two hosts on which mites initially showed both high juvenile mortality and low acceptance, tomato and broccoli. In less than ten generations, mites from the line kept on each host showed both lower mortality and greater acceptance on it than mites from a control line kept on lima bean, a favorable host for T. urticae. Host acceptance was measured by the proportion of mites attempting to disperse from leaves of the host. The line kept on tomato but not the one kept on broccoli also increased in development rate on its host. These results and those of a similar previous experiment on cucumber indicate that T. urticae populations can adapt to a diversity of initially unfavorable hosts. T. urticae populations therefore should be able to respond to temporal and spatial variation in host availability by adapting to the most abundant hosts.     

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.     

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.     

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.     

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.     

Evaluation of airborne methyl salicylate for improved conservation biological control of two-spotted spider mite and hop aphid in Oregon hop yards

The use of synthetic herbivore-induced plant volatiles (HIPV) to attract natural enemies has received interest as a tool to enhance conservation biological control (CBC). Methyl salicylate (MeSA) is a HIPV that is attractive to several key predators of two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), and hop aphid, Phorodon humuli (Schrank) (Homoptera: Aphididae). A 2-year study was conducted to evaluate the recommended commercial use of MeSA in hop yards in Oregon. Slow-release MeSA dispensers were stapled to supporting poles in 0.5 ha plots and these plots were compared to a paired non-treated plot on each of three farms in 2008 and 2009. Across both years, there was a trend for reduced (range 40–91%) mean seasonal numbers of T. urticae in five of the six MeSA-baited plots. Stethorus spp., key spider mite predators, tended to be more numerous in MeSA-baited plots compared to control plots on a given farm. Mean seasonal densities of hop aphid and other natural enemies (e.g., Orius spp. and Anystis spp.) were similar between MeSA-treated and control plots. Variability among farms in suppression of two-spotted spider mites and attraction of Stethorus spp. suggests that the use of MeSA to enhance CBC of spider mites in commercial hop yards may be influenced by site-specific factors related to the agroecology of individual farms or seasonal effects that require further investigation. The current study also suggests that CBC of hop aphid with MeSA in this environment may be unsatisfactory.     

Lima bean�Clady beetle interactions: spider mite mediates sublethal effects of its host plant on growth and development of its predator

Cultivated plants can have negative effects on natural enemies that attack spider mites. In this study, we tested the hypothesis that spider mites mediate effects of a lima bean, Phaseolus lunatus L., cultivar on the life history of a lady beetle Stethorus punctillum Weise. We provisioned laboratory arenas with two-spotted spider mites, Tetranychus urticae Koch, from planters containing Henderson Bush Bean or Fordhook 242 lima bean plants and monitored the growth, development, larval survival, fecundity, and adult life span of predators. We determined the protein content and the linamarin (a cyanogenic glycoside) content in foliage, spider mites, and predators. Predators took longer to develop and were smaller sized when consuming mites from the Henderson foliage. There was no significant mite-mediated effect of cultivar on predator fecundity or life span. Although soluble protein was greater in foliage of the Henderson than the Fordhook cultivar, mites contained less protein when reared on the Henderson, and predators contained less protein when fed with mites from the Henderson. Linamarin content was greater in Henderson than Fordhook foliage, and greater in spider mites and predators in the Henderson treatment. Linamarin in Henderson foliage may reduce the ability of spider mites to utilize plant protein. As a result, prey quality is reduced and predators that feed on these prey (from the Henderson treatment) grow at a slower rate and are smaller sized than their cohorts (from the Fordhook treatment). In conclusion, T. urticae mediates the effects of the Henderson cultivar on S. punctillum development but not fecundity or life span.     

Predation by Allothrombium pulvinum on the spider mites Tetranychus urticae and Amphitetranychus viennensis: Predation Rate, Prey Preference and Functional Response

The deutonymphs of Allothrombium pulvinum Ewing (Acari: Trombidiidae) are among the most important natural enemies of spider mites in North, North East and West Iran. In this study, maximum predation rate and preference experiments were conducted with A. pulvinum deutonymphs on apple leaf discs, to determine their preference for either of two spider mite species: Amphitetranychus viennensis (Zacher) and Tetranychus urticae Koch (Acari: Tetranychidae). Maximum predation rate tests showed that the predatory mite consumed more eggs and females of T. urticae than of A. viennensis. Furthermore, the Manly’s preference index for eggs and females of T. urticae confirmed that T. urticae were the preferred prey. The functional response of A. pulvinum deutonymphs on females of T. urticae was examined over a 24-h period. Predation of A. pulvinum deutonymphs presented with females of T. urticae followed a type III functional response. Estimated handling time for the predatory mites was 4.51 h and attack coefficient b, which describes the changes in attack rate with prey densities in a type III functional response, was 0.021.     

Species- and density-dependent induction of volatile organic compounds by three mite species in cassava and their role in the attraction of a natural enemy

Upon damage by herbivores, plants induce an array of volatile organic compounds (VOCs) that mediate ecological interactions involving communication with organisms of the second and third trophic levels. VOC-mediated tritrophic interactions have largely been studied in various systems, including cassava (Manihot esculenta), but little is known about the chemical nature of herbivore-induced VOCs in this crop and the response they evoke in natural enemies. Several tetranychid and predatory mites are associated with cassava. Here, VOC emissions from uninfested plants and plants infested with 200 or 400 Mononychellus tanajoa, a specialist herbivore on cassava, and the generalists Tetranychus urticae and T. gloveri were measured. Dual-choice experiments were also conducted to assess the preference of inexperienced (reared on prey-infested bean plants) and experienced (adapted on prey-infested cassava plants) predatory mites, Neoseiulus idaeus (Phytoseiidae), between odors of uninfested plants versus odors of plants infested with M. tanajoa, T. urticae or T. gloveri. Two hundred individuals significantly increased the emissions of (Z)-3-hexen-1-ol, (E)-β-ocimene, β-caryophyllene, alloaromadendrene and (E)-geranyl acetone in T. urticae-infested plants, and (E)-β-ocimene and methyl salicylate (MeSA) in T. gloveri-infested plants. Four hundred individuals significantly increased the emissions of (Z)-3-hexen-1-ol, MeSA, α-pinene and D-limonene in M. tanajoa-infested plants. In addition, T. urticae at this density induced (E)-β-ocimene, D-limonene, (E)-geranyl acetone and six compounds that were not detected in other treatments. Tetranychus gloveri-infested plants induced the emissions of (E)-2-hexenal and D-limonene. Regardless of the infesting species, inexperienced N. idaeus did not discriminate between uninfested or infested plants. Upon experience, they discriminated between the odors of uninfested and T. urticae-damaged plants. Our findings reveal that mite infestations in cassava result in density-dependent and species-specific emission of VOCs, and that N. idaeus relies on associative learning to forage for its prey.     

An ecological cost of plant defence: attractiveness of bitter cucumber plants to natural enemies of herbivores

Plants produce defences that act directly on herbivores and indirectly via the attraction of natural enemies of herbivores. We examined the pleiotropic effects of direct chemical defence production on indirect defence employing near‐isogenic varieties of cucumber plants (Cucumis sativus) that differ qualitatively in the production of terpenoid cucurbitacins, the most bitter compounds known. In release–recapture experiments conducted in greenhouse common gardens, blind predatory mites were attracted to plants infested by herbivorous mites. Infested sweet plants (lacking cucurbitacins), however, attracted 37% more predatory mites than infested bitter plants (that produce constitutive and inducible cucurbitacins). Analysis of the headspace of plants revealed that production of cucurbitacins was genetically correlated with large increases in the qualitative and quantitative spectrum of volatile compounds produced by plants, including induced production of (E )‐β‐ocimene (3E )‐4,8‐dimethyl‐1,3,7‐nonatriene, (E,E)‐α‐farnesene, and methyl salicylate, all known to be attractants of predators. Nevertheless, plants that produced cucurbitacins were less attractive to predatory mites than plants that lacked cucurbitacins and predators were also half as fecund on these bitter plants. Thus, we provide novel evidence for an ecological trade‐off between direct and indirect plant defence. This cost of defence is mediated by the effects of cucurbitacins on predator fecundity and potentially by the production of volatile compounds that may be repellent to predators.     

Attraction of a predator to chemical information related to nonprey: when can it be adaptive?

Information specificity can be important to animals in makingoptimal decisions. However, it is not always necessary to useevery level of specificity. We analyzed the response of thepredatory mite Phytoseiulus persimilis to plant-produced informationrelated to a nonprey herbivore. This predator is a specialistfeeding on spider mites in the genus Tetranychus. Caterpillarsof Spodoptera exigua cannot serve as prey. Plants respond toan infestation by herbivores with the emission of volatilesthat attract carnivorous enemies of the herbivores. Conspecific plants infested with different herbivore species can emit blendsthat are qualitatively identical, while differing in the ratiosof blend components. However, different plant species emitvolatile blends that differ qualitatively. We demonstratedthat the predator P. persimilis is attracted to volatiles frombean plants infested with S. exigua caterpillars, but thatthis attraction is affected by predator starvation and host-plantexperience. One-hour and 24-h starved predators were made to represent predators that just lost a prey patch versus predatorsthat have totally lost a prey patch. Predators reared on spidermites on bean were attracted to bean plants infested with caterpillarswhen starved for 1 h but not when starved for 24 h. Both predatorgroups were attracted to bean plants infested with prey (i.e.,spider mites). One-hour starved predators can use the odorto relocate the rewarding prey patch they just lost contactwith, and using a general olfactory representation of the blendis sufficient for relocation. In contrast, for 24-h starvedpredators, the perception of a plant's odor blend is unlikelyto represent the prey patch lost, and discriminating betweenan odor blend representing prey or nonprey will avoid investingtime in finding a nonprey herbivore. In contrast, predatorsthat had been reared on spider mites on cucumber and thus hadexperienced a qualitatively different odor blend were not attractedto volatiles from caterpillar-infested bean plants. They wereattracted to spider mite-infested bean plants, irrespectiveof starvation level. To cucumber-experienced predators, theperception of bean plant odor cannot represent the prey patch lost, but only a new prey patch. Being discriminative and onlyresponding to prey-infested plants is adaptive in this situation.Our results are discussed in the context of optimal informationprocessing.     

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.     

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.