Maarten A. Posthumus

PLANT STRATEGIES OF MANIPULATING PREDATOR- PREY INTERACTIONS THROUGH ALLELOCHEMICALS: PROSPECTS FOR APPLICATION IN PEST CONTROL

To understand the role of allelochemicals in predator-prey interactions it is not sufficient to study the behavioral responses of predator and prey. One should elucidate the origin of the allelochemicals and be aware that it may be located at another trophic level. These aspects are reviewed for predator-prey interactions in general and illustrated in detail for interactions between predatory mites and herbivorous mites. In the latter system there is behavioral and chemical evidence for the involvement of the host plant in production of volatile allelochemicals upon damage by the herbivores with the consequence of attracting predators. These volatiles not only influence predator behavior, but also prey behavior and even the attractiveness of nearby plants to predators. Herbivorous mites disperse away from places with high concentrations of the volatiles, and undamaged plants attract more predators when previously exposed to volatiles from infested conspecific plants rather than from uninfested plants. The latter phenomenon may well be an example of plant-to-plant communication. The involvement of the host plant is probably not unique to the predator-herbivore-plant system under study. It may well be widespread since it makes sense from an evolutionary point of view. If so, prospects for application in pest control are wide open. These are discussed, and it is concluded that crop protection in the future should include tactics whereby man becomes an ally to plants in their strategies to manipulate predator-prey interactions through allelochemicals.

Isolation and identification of volatile kairomone that affects acarine predator-prey interactions: involvement of host plant in its production.

A volatile kairomone emitted from lima bean plants (Phaseolus lunatus) infested with the spider miteTetranychus urticae, was collected on Tenax-TA and analyzed with GC-MS. Two components were identified as the methylene monoterpene (3E)-4,8-dimethyl-1,3,7-nonatriene and the methylene sesquiterpene (3E,7E)-4,8,12-dimethyl-1,3,7,11-tridecatetraene, respectively, after purification by preparative GC on a megabore column and recording of UV, IR, and [1H]NMR spectra. The response of two species of predatory mites towards the identified chemicals was tested in a Y-tube olfactometer. Four of the compounds tested, linalool (3,7-dimethyl-1,6-octadien-3-ol), (E)-β-ocimene [(3E)-3,7-dimethyl-1,3,6-octatriene], (3E)-4,8-dimethyI-1,3,7-nonatriene, and methyl salicylate attracted females ofPhytoseiulus persimilis. Linalool and methyl salicylate attracted females ofAmblyseius potentillae. The response ofA. potentillae to these two kairomone components was affected by the rearing diet of the predators in the same way as was reported for the response to the natural kairomone blend: when reared on a carotenoid-deficient diet, the predators responded to the volatile kairomone ofT. urticae, but when reared on a carotenoid-containing diet they did not. The identified kairomone components are all known from the plant kingdom. They are not known to be produced by animals de novo. In addition to biological evidence, this chemical evidence suggests that the plant is involved in production of the kairomone. Based on the present study and literature data on the response ofT. urticae to infochemicals, it is concluded that the kairomone component linalool is also a component of a volatile spider-mite dispersing pheromone.

Jasmonic Acid and Herbivory Differentially Induce Carnivore-Attracting Plant Volatiles in Lima Bean Plants

Lima bean plants respond to feeding damage of two-spotted spider mites (Tetranychus urticae) with the emission of a complex blend of volatiles that are products of several different biosynthetic pathways. These volatiles attract the carnivorous mite Phytoseiulus persimilis, a specialist predator of the spider mites that exterminates entire prey populations, and thus the volatiles contribute indirectly to plant defense. The volatile blend constitutes information to the carnivores, and blend composition is an important factor in this. Jasmonic acid (JA) is involved in the signal transduction of this induced defense. Application of JA through the petiole of Lima bean plants induces a volatile blend that is similar, but not identical, to that emitted by spider mite-infested plants. The induced volatiles originate from the lipoxygenase pathway, the shikimic acid pathway, and the isoprenoid pathway. Among the induced bean plant volatiles are nitriles and oximes. Of a total of 61 components, 10 are emitted at significantly different rates. Among these are the terpene (E)-4,8-dimethyl-1,3,7-nonatriene and the phenolic methyl salicylate, two compounds that are known to attract P. persimilis. A crucial test for comparing the effect of spider mite damage and JA application on volatile induction is the response of P. persimilis. The carnivore is attracted by volatiles from JA-treated plants. Moreover, even treatment of Lima bean plants with methyl jasmonate vapor made the plants attractive to the carnivorous mites. However, the predators prefer the volatiles from spider-mite-infested Lima bean plants over those from JA-treated plants. Thus, chemical as well as behavioral analyses demonstrate that spider mite damage and JA treatment have similar, although not identical, effects on volatile induction in Lima bean plants.

Volatile herbivore-induced terpenoids in plant-mite interactions: Variation caused by biotic and abiotic factors

Plants may defend themselves against herbivores by enhancing the effectiveness of natural enemies of herbivores. This is termed “indirect defense,” which may be induced by herbivore damage. An important aspect of induced indirect defense is the attraction of the herbivores natural enemies to infested plants by the plant emitting so-called “herbivore-induced synomone” (HIS) in response to herbivore damage. In this paper, we review the role of terpenoids in the induced indirect defense of plants against herbivorous mites. HIS are emitted from both damaged and undamaged areas of infested plants, and the composition of HIS varies among different plant species. The emission of HIS may also vary within a plant species, depending upon: (1) plant cultivar, (2) leaf growth stage, (3) the herbivore species that is attacking, and (4) abiotic conditions (light intensity, time of year, and water stress). Predatory mites cope with this variation of HIS by innate recognition as well as temporary specialization to a certain HIS via learning.

Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula : Chemical, behavioral, and gene-expression analysis

Many plant species defend themselves against herbivorous insects indirectly by producing volatiles in response to herbivory. These volatiles attract carnivorous enemies of the herbivores. Research on the model plant Arabidopsis thaliana (L.) Heynh. has contributed considerably to the unraveling of signal transduction pathways involved in direct plant defense mechanisms against pathogens. Here, we demonstrate that Arabidopsis is also a good candidate for studying signal transduction pathways involved in indirect defense mechanisms by showing that: (1) Adult females of Cotesia rubecula, a specialist parasitic wasp of Pieris rapae caterpillars, are attracted to P. rapae-infested Arabidopsis plants. (2) Arabidopsis infested by P. rapae emits volatiles from several major biosynthetic pathways, including terpenoids and green leaf volatiles. The blends from herbivore-infested and artificially damaged plants are similar. However, differences can be found with respect to a few components of the blend, such as two nitriles and the monoterpene myrcene, that were produced exclusively by caterpillar-infested plants, and methyl salicylate, that was produced in larger amounts by caterpillar-infested plants. (3) Genes from major biosynthetic pathways involved in volatile production are induced by caterpillar feeding. These include AtTPS10, encoding a terpene synthase involved in myrcene production, AtPAL1, encoding phenylalanine ammonia-lyase involved in methyl salicylate production, and AtLOX2 and AtHPL, encoding lipoxygenase and hydroperoxide lyase, respectively, both involved in the production of green leaf volatiles. AtAOS, encoding allene oxide synthase, involved in the production of jasmonic acid, also was induced by herbivory.

Developmental stage of herbivorePseudaletia separata affects production of herbivore-induced synomone by corn plants.

The female parasitic waspCotesia kariyai discriminated between the volatiles of corn leaves infested by younger host larvaePseudaletia separata (first to fourth instar) and uninfested leaves in a Y-tube olfactometer; the wasps were attracted to the infested leaves. In contrast, when corn plants were infested by the later stages (fifth and sixth instar) of the armyworm, the wasps did not distinguish between infested corn leaves and uninfested corn leaves in the olfactometer. Mechanically damaged leaves were no more attractive than undamaged leaves, and host larvae or their feces were not attractive to the parasitoid. Through chemical analysis, the herbivore-induced plant volatiles were identified in the headspace of infested corn leaves. The herbivore-induced volatiles (HIVs) constituted a larger proportion of the headspace of corn leaves infested by early instar armyworms than of corn leaves infested by late instar armyworms. Application of third-instar larval regurgitant onto artificially damaged sites of leaves resulted in emission of parasitoid attractants from the leaf, whereas leaves treated with sixth-instar regurgitant did not. The function of this herbivore-stage related specificity of herbivore-induced synomones is discussed in a tritrophic context.

ATTRACTION OF COLORADO POTATO BEETLE TO HERBIVORE-DAMAGED PLANTS DURING HERBIVORY AND AFTER ITS TERMINATION

Large, undamaged potato plants (>60 cm, 5–6 weeks old) attract the Colorado potato beetle (Leptinotarsa decemlineata), but small potato plants (15–25 cm high, 2–3 weeks old) do not. However, small plants become attractive to CPB when they are damaged. Mechanical damage inflicted with scissors results in short-term (lasting less than 15 min) attraction, while more severe damage with carborundum powder results in a longer lasting attraction (at least 1 hr). CPB adults are also attracted to small plants infested with CPB and Spodoptera exigua larvae. After the larvae had been removed for 50 min following a short duration (30 min) of feeding, CPB adults were no longer attracted to the plants. However, when CPB larvae had been removed after they had fed for 60–90 min, the plants were somewhat attractive to the beetles, although significantly less than they had been when the larvae were feeding. Attraction increased with time after feeding ceased. Furthermore, beetles were strongly attracted to plants 50 min after larvae were removed when the plants had been fed upon by larvae for 18–24 hr. Thus it appears that there are two stages of attraction, first, to volatiles released directly from the wound site, and second, to volatiles that are induced in response to herbivory. Chemical analyses of the headspace of infested potato plants show that infestation results in the emission of a mixture of chemicals that is qualitatively quite similar to that emitted by undamaged plants. The major components of the mixture are that emitted by undamaged plants. The major components of the mixture are terpenoids and fatty acid derivatives such as aldehydes and alcohols. The emission rate of some of these chemicals declines after removal of the beetles, while the emission rate of other chemicals increases with the duration of beetle feeding and remains at a high level even after removal of the beetles. Thus, the composition of the mixture changes temporally during and after herbivore feeding, which may explain the recorded behavior of the beetles.

Variation in composition of predator-attracting allelochemicals emitted by herbivore-infested plants: Relative influence of plant and herbivore

SummaryDuring foraging, natural enemies of herbivores may employ volatile allelochemicals that originate from an interaction of the herbivore and its host plant. The composition of allelochemical blends emitted by herbivore-infested plants is known to be affected by both the herbivore and the plant. Our chemical data add new evidence to the recent notion that the plants are more important than the herbivore in affecting the composition of the volatile blends. Blends emitted by apple leaves infested with spider mites of 2 different species,T. urticae andP. ulmi, differed less in composition (principally quantitative differences for some compounds) than blends emitted by leaves of two apple cultivars infested by the same spider-mite species,T. urticae (many quantitative and a few qualitative differences). Comparison between three plant species — apple, cucumber and Lima bean — reveals even larger differences between volatile blends emitted upon spider-mite damage (many quantitative differences and several qualitative differences).

Induction of parasitoid attracting synomone in brussels sprouts plants by feeding ofPieris brassicae larvae: Role of mechanical damage and herbivore elicitor.

Induction of plant defense in response to herbivory includes the emission of synomones that attract the natural enemies of herbivores. We investigated whether mechanical damage to Brussels sprouts leaves (Brassica oleracea var.gemmifera) is sufficient to obtain attraction of the parasitoidCotesia glomerata or whether feeding byPieris brassicae caterpillars elicits the release of synomones not produced by mechanically damaged leaves. The response of the parasitoidCotesia glomerata to different types of simulated herbivory was observed. Flight-chamber dual-choice tests showed that mechanically damaged cabbage leaves were less attractive than herbivore-damaged leaves and mechanically damaged leaves treated with larval regurgitant. Chemical analysis of the headspace of undamaged, artificially damaged, caterpillar-infested, and caterpillar regurgitant-treated leaves showed that the plant responds to damage with an increased release of volatiles. Greenleaf volatiles and several terpenoids are the major components of cabbage leaf headspace. Terpenoids are emitted in analogous amounts in all treatments, including undamaged leaves. On the other hand, if the plant is infested by caterpillars or if caterpillar regurgitant is applied to damaged leaves, the emission of green-leaf volatiles is highly enhanced. Our data are in contrast with the induction of more specific synomones in other plant species, such as Lima bean and corn.

Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families.

Many plant species are known to emit herbivore-induced volatiles in response to herbivory. The spider mite Tetranychus urticae Koch is a generalist that can feed on several hundreds of host plant species. Volatiles emitted by T. urticae-infested plants of 11 species were compared: soybean (Glycine max), golden chain (Laburnum anagyroides), black locust (Robinia pseudo-acacia), cowpea (Vigna unguiculata), tobacco (Nicotiana tabacum), eggplant (Solanum melalonga), thorn apple (Datura stramonium), sweet pepper (Capsicum annuum), hop (Humulus lupulus), grapevine (Vitis vinifera), and ginkgo (Ginkgo biloba). The degree to which the plant species produced novel compounds was analyzed when compared to the odors of mechanically damaged leaves. Almost all of the investigated plant species produced novel compounds that dominated the volatile blend, such as methyl salicylate, terpenes, oximes, and nitriles. Only spider mite-infested eggplant and tobacco emitted a blend that was merely quantitatively different from the blend emitted by mechanically damaged or clean leaves. We hypothesized that plant species with a low degree of direct defense would produce more novel compounds. However, although plant species with a low direct defense level do use indirect defense to defend themselves, they do not always emit novel compounds. Plant species with a high level of direct defense seem to invest in the production of novel compounds. When plant species of the Fabaceae were compared to plant species of the Solanaceae, qualitative differences in spider mite-induced volatile blends seemed to be more prominent in the Fabaceae than in the Solanaceae.