Specific herbivore-induced volatiles defend plants and determine insect community composition in the field.

In response to insect attack, plants release complex blends of volatile compounds. These volatiles serve as foraging cues for herbivores, predators and parasitoids, leading to plant-mediated interactions within and between trophic levels. Hence, plant volatiles may be important determinants of insect community composition. To test this, we created rice lines that are impaired in the emission of two major signals, S-linalool and (E)-ß-caryophyllene. We found that inducible S-linalool attracted predators and parasitoids as well as chewing herbivores, but repelled the rice brown planthopper Nilaparvata lugens, a major pest. The constitutively produced (E)-ß-caryophyllene on the other hand attracted both parasitoids and planthoppers, resulting in an increased herbivore load. Thus, silencing either signal resulted in specific insect assemblages in the field, highlighting the importance of plant volatiles in determining insect community structures. Moreover, the results imply that the manipulation of volatile emissions in crops has great potential for the control of pest populations.

Attraction of a leaf beetle (Oreina cacaliae) to damaged host plants.

Early in spring, just after the snow melts, the leaf beetle Oreina cacaliae feeds on flowers of Petasites paradoxus. Later in spring they switch to their principle host plant Adenostyles alliariae. The attractiveness of short- and long-term damaged host plants was studied in a wind tunnel. The spring host P. paradoxus was more attractive to the beetles after it had been damaged overnight by conspecifics or artificially, but not when the plants were damaged half an hour before the wind-tunnel experiments. Contrary to P. paradoxus, the principle host plant, A. alliariae was more attractive shortly after an attack by conspecifics (half an hour before the experiment) compared to a undamaged plant, but lost its increased attractiveness when damaged overnight. The enhanced attraction of damaged plants was longer lasting in the spring host P. paradoxus than in the main host A. alliariae. Volatiles emitted by host plants were collected and gas chromatographic analyses of the odors collected showed qualitative and quantitative differences between damaged and undamaged plants. Among the volatiles recorded, green leaf volatiles and mono- and sesquiterpenes dominated. In overnight damaged P. paradoxus plants with an enhanced attractiveness, limonene was emitted in higher amounts. In freshly damaged A. alliariae leaves, more alpha-humulene and germacrene D were emitted compared to (E,E)-alpha-farnesene, whereas in the less attractive A. alliariae plants, more (E,E)-alpha-farnesene was emitted compared to alpha-humulene and germacrene D. In the field, the long lasting attraction of flowering P. paradoxus early in the season may facilitate mating in O. cacaliae after a successful overwintering.

Parasitoids may determine plant fitness--a mathematical model based on experimental data.

The present paper deals with the problem of enhancement of plant fitness due to parasitization of herbivores. The experimental evidence for such situations is reviewed. Two mathematical models, plant-herbivore (two trophic) and plant-herbivore-parasitoid (three trophic) are considered to analyse the experimental observations. The effect of environmental fluctuation in the tritrophic system is also observed and optimum values of the inaccessible parameters involved in the system are estimated for purposes of biological control.

Attraction of parasitic wasps by caterpillar-damaged plants.

Plant volatiles emitted in response to herbivory have been suggested to function as signals to attract natural enemies of herbivores. Most known examples of induced plant volatiles used by natural enemies involve parasitoids that locate caterpillars by means of odours emitted by plants after caterpillar attack. We study the tritrophic system that comprises the parasitoid Cotesia marginiventris, host caterpillars from the genus Spodoptera, and maize plants. Among the volatiles emitted by caterpillar-damaged maize plants, sesquiterpenes and indole are particularly attractive to the parasitoid. The usefulness of these plant volatiles for parasitoids is obvious. Less clear is their benefit to plants that emit them, as in most cases parasitization does not immediately stop caterpillars from damaging plants. However, plants appear to benefit directly from attracting C. marginiventris, as parasitized caterpillars consume considerably less plant tissue than unparasitized caterpillars. It is expected that in systems where parasitoids significantly reduce herbivory, they have contributed to selective pressures that have shaped the phenomenon of herbivore-induced volatile emissions by plants.

How caterpillar-damaged plants protect themselves by attracting parasitic wasps.

Parasitic and predatory arthropods often prevent plants from being severely damaged by killing herbivores as they feed on the plants. Recent studies show that a variety of plants, when injured by herbivores, emit chemical signals that guide natural enemies to the herbivores. It is unlikely that herbivore-damaged plants initiate the production of chemicals solely to attract parasitoids and predators. The signaling role probably evolved secondarily from plant responses that produce toxins and deterrents against herbivores and antibiotics against pathogens. To effectively function as signals for natural enemies, the emitted volatiles should be clearly distinguishable from background odors, specific for prey or host species that feed on the plant, and emitted at times when the natural enemies forage. Our studies on the phenomena of herbivore-induced emissions of volatiles in corn and cotton plants and studies conducted by others indicate that (i) the clarity of the volatile signals is high, as they are unique for herbivore damage, produced in relatively large amounts, and easily distinguishable from background odors; (ii) specificity is limited when different herbivores feed on the same plant species but high as far as odors emitted by different plant species and genotypes are concerned; (iii) the signals are timed so that they are mainly released during the daytime, when natural enemies tend to forage, and they wane slowly after herbivory stops.

The chemistry of eavesdropping, alarm, and deceit.

Arthropods that prey on or parasitize other arthropods frequently employ those chemical cues that reliably indicate the presence of their prey or hosts. Eavesdropping on the sex pheromone signals emitted to attract mates allows many predators and parasitoids to find and attack adult insects. The sex pheromones are also useful signals for egg parasitoids since eggs are frequently deposited on nearby plants soon after mating. When the larval stages of insects or other arthropods are the targets, a different foraging strategy is employed. The larvae are often chemically inconspicuous, but when they feed on plants the injured plants respond by producing and releasing defensive chemicals. These plant chemicals may also serve as "alarm signals" that are exploited by predators and parasitoids to locate their victims. There is considerable evidence that the volatile "alarm signals" are induced by interactions of substances from the herbivore with the damaged plant tissue. A very different strategy is employed by several groups of spiders that remain stationary and send out chemical signals that attract prey. Some of these spiders prey exclusively on male moths. They attract the males by emitting chemicals identical to the sex pheromones emitted by female moths. These few examples indicate the diversity of foraging strategies of arthropod predators and parasitoids. It is likely that many other interesting chemically mediated interactions between arthropod hunters and their victims remain to be discovered. Increased understanding of these systems will enable us to capitalize on natural interactions to develop more ecologically sound, environmentally safe methods for biological control of insect pests of agriculture.

Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plant.

Cotton plants attacked by herbivorous insect pests emit relatively large amounts of characteristic volatile terpenoids that have been implicated in the attraction of natural enemies of the herbivores. However, the composition of the blend of volatile terpenes released by the plants varies remarkably throughout the photoperiod. Some components are emitted in at least 10-fold greater quantities during the photophase than during the scotophase, whereas others are released continuously, without conforming to a pattern, during the entire time that the plants are under herbivore attack. The diurnal pattern of emission of volatile terpenoids was determined by collecting and analyzing the volatile compounds emitted by cotton plants subjected to feeding damage by beet armyworm larvae in situ. The damage was allowed to proceed for 3 days, and volatile emission was monitored continuously. During early stages of damage high levels of lipoxygenase-derived volatile compounds [e.g., (Z)-3-hexenal, (Z)-3-hexenyl acetate] and several terpene hydrocarbons [e.g., alpha-pinene, caryophyllene] were emitted. As damage proceeded, high levels of other terpenes, all acyclic [e.g., (E)-beta-ocimene, (E)-beta-farnesene], were emitted in a pronounced diurnal fashion; maximal emissions occurred in the afternoon. These acyclic terpenes followed this diurnal pattern of emission, even after removal of the caterpillars, although emission was in somewhat smaller amounts. In contrast, the emission of cyclic terpenes almost ceased after the caterpillars were removed.

Herbivore-induced volatile emissions from cotton (Gossypium hirsutum L.) seedlings.

The effect of herbivory on the composition of the volatile blends released by cotton seedlings was investigated by collecting volatiles from undamaged, freshly damaged (0-2 hr after initiation of feeding), and old damaged (16-19 hr after initiation of feeding) plants on which corn earworm caterpillars (Helicoverpa zea Boddie) were actively feeding. A blend of 22 compounds was consistently observed to be emitted by the old damaged plants with nine occurring either only in, or in significantly greater amounts in old damaged, as compared with freshly damaged plants. These were (Z)-3-hexenyl acetate, hexyl acetate, (E)-ß-ocimene, (3E)-4,8-dimethyl-1,3,7-nonatriene, (Z)-3-hexenyl butyrate, (E)-2-hexenyl butyrate, (Z)-3-hexenyl 2-methylbutyrate, (E)-2-hexenyl 2-methylbutyrate, and indole. The nature of this response is compared with other studies where herbivore-induced volatile responses are also known. The presence of large amounts of terpenes and aldehydes seen at the onset of feeding and the appearance of other compounds hours later suggest that cotton defense mechanisms may consist of a constitutive repertoire that is augmented by an induced mechanism mobilized in response to attack. A number of the induced compounds are common to many plants where, in addition to an immediate defensive function, they are known to be involved in the attraction of natural enemies.

An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps.

Regurgitate of corn-fed beet armyworm (BAW) caterpillars,Spodoptera exigua, when applied to damaged sites of corn (Zea mays) seedlings, causes the release of relatively large amounts of terpenes by the seedlings several hours later. This plant response could be induced by merely placing the cut stem of seedlings in a solution of BAW regurgitate for 12 hr, a response that could not be induced by placing seedlings in water only. Regurgitate of BAW fed various diets, including a minimal diet of filter paper, were all active. However, seedlings placed in corn leaf juice, BAW hemolymph, or BAW feces extract released significantly smaller amounts of terpenes than did seedlings placed in BAW regurgitate. These results indicate that the active components are present in relatively large concentrations in regurgitate and that they are not related to the food source. Furthermore, regurgitate from several other species of caterpillars (Spodoptera frugiperda, Helicoverpa zea,Trichoplusia ni, andAnticarsia gemmatalis) as well as from the grasshopperSchistocerca americana induced the release of significant amounts of terpenes in corn seedlings. The release of these volatiles, therefore, appears to be a general response to attack by phytophagous insects. The terpene-releasing corn seedlings were highly attractive to the generalist parasitoidCotesia marginiventris and to the specialized parasitoidMicroplitis croceipes. This study confirms a systemic herbivore-elicited release of terpenes in corn. It is proposed that such chemicals serve multifunctional purposes that directly and indirectly protect plants against herbivorous arthropods and pathogens.

Systemic release of chemical signals by herbivore-injured corn.

Corn seedlings respond to insect herbivore-inflicted injury by releasing relatively large amounts of several characteristic terpenoids and, as a result, become highly attractive to parasitic wasps that attack the herbivores. Chemical evidence showed that the induced emission of volatiles is not limited to the sites of damage but occurs throughout the plant. This evidence was obtained by comparing the release of volatiles from leaves of unharmed (control) seedlings with the release of volatiles from undamaged leaves of seedlings with two injured leaves treated with caterpillar regurgitant. Immediately after injury no differences were measured in the released volatiles, but several hours later the undamaged leaves of injured plants released the terpenoids linalool, (3E)-4,8-dimethyl-1,3,7-nonatriene, and (3E,7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene in significantly larger amounts than leaves of unharmed plants. Other volatiles that are released by herbivore-injured leaves were detected occasionally only in trace amounts from the undamaged leaves of a damaged seedling. The systemic release of volatiles by injured corn coincided with attractiveness to the parasitoid Cotesia marginiventris; undamaged leaves of injured plants became significantly more attractive than leaves from control seedlings. These findings show conclusively that when a plant is injured by an insect herbivore the whole plant emits chemical signals.

Isolation and identification of allelochemicals that attract the larval parasitoid,Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts.

Volatiles released from corn seedlings on which beet armyworm larvae were feeding were attractive to females of the parasitoid,Cotesia marginiventris (Cresson), in flight tunnel bioassays. Analyses of the collected volatiles revealed the consistent presence of 11 compounds in significant amounts. They were: (Z)-3-hexenal, (E)-2-hexenal, (Z)-3-hexen-1-ol, (Z)- 3-hexen-1-yl acetate, linalool, (3E)-4,8-dimethyl-1,3,7-nonatriene, indole, α-trans-bergamotene, (E)-ß-farnesene, (E)-nerolidol, and (3E,7E)-4,8,12-trimethyl-1, 3,7,ll-tridecatetraene. A synthetic blend of all 11 compounds was slightly less attractive to parasitoid females than an equivalent natural blend. However, preflight experience with the synthetic blend instead of experience with a regular plant-host complex significantly improved the response to the synthetic blend. Our results suggest thatC. marginiventris females, in their search for hosts, use a blend of airborne semiochemicals emitted by plants on which their hosts feed. The response to a particular odor blend dramatically increases after a parasitoid experiences it in association with contacting host by-products.

Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps.

Corn seedlings release large amounts of terpenoid volatiles after they have been fed upon by caterpillars. Artificially damaged seedlings do not release these volatiles in significant amounts unless oral secretions from the caterpillars are applied to the damaged sites. Undamaged leaves, whether or not they are treated with oral secretions, do not release detectable amounts of the terpenoids. Females of the parasitic wasp Cotesia marginiventris (Cresson) learn to take advantage of those plant-produced volatiles to locate hosts when exposed to these volatiles in association with hosts or host by-products. The terpenoids may be produced in defense against herbivores but may also serve a secondary function in attracting the natural enemies of these herbivores.

How contact foraging experiences affect preferences for host-related odors in the larval parasitoidCotesia marginiventris (Cresson) (Hymenoptera: Braconidae).

Responses of individual females of the parasitoidCotesia marginiventris to the odors of four different complexes of host larvae feeding on leaves were observed in a four-arm olfactometer. The plant-host complexes were composed of fall armyworm (FAW) larvae or cabbage looper (CL) larvae feeding on either corn or cotton seedlings. Prior to testing, each female was given a brief foraging experience on a plant-host complex and was then exposed to the odors of the same complex in the olfactometer. The experienced females responded to familiar odors in a dose-related manner, and these responses were virtually identical to all four complexes. Preferences for the odors of one of two plant-host complexes were tested in dual choice situations. Generally, FAW odors were preferred over CL odors and corn odors over cotton odors. A short foraging experience significantly affected the females' odor preferences in favor of the odors released by the experienced complex. Additional experiments revealed that neither longer bouts of experience nor bouts that included ovipositions resulted in a stronger change in preference. Experience affected preference in combinations where only the host species was varied as well as in combinations where only the plant species was varied. The results, therefore, strongly indicate that both the plants and the hosts somehow are involved in the production and/or release of the semiochemicals that attractC. marginiventris.

The function of host discrimination and superparasitization in parasitoids.

Host discrimination, i.e. the ability to distinguish unparasitized hosts from parasitized ones, and to reject the latter for egg laying is present in many parasitic wasp species. This property is classically considered as an example of contest competition, and is supposed to have a number of functions. However, different species do not react to each other's marks and lay eggs in hosts parasitized by the other species. Apparently the marks used for recognition are specific.Multiparasitization is the best strategy when hosts are scarce and the egg supplies of the parasitoids are not limited. Interspecific host discrimination is not an ESS.Superparasitization within one species would have selective advantage if the number of unparasitized hosts is small and the wasp has a reasonable chance to lay her egg in a host that is not parasitized by herself, and if the chance for her offspring to survive the competitive battle with the first parasitoid larva is not too small. This is shown to be the case.However, marks are not individual and wasps cannot distinguish hosts parasitized by themselves from those parasitized by others. The hypothesis is tested that the egg laying strategy (i.e. the decision to superparasitize) of wasps is dependent on the number of conspecifics that is searching simultaneously for hosts, since this determines the chance that a parasitized host encountered by a wasp is parasitized by herself.It is shown that host discrimination cannot be regarded as a case of contest competition. Other aspects of superparasitization, related to interference and population regulation, sex allocation and encapsulation are briefly discussed.