Turlings, Ted

2000, Turlings, Ted, Alborn, Hans, Loughrin, John H, Tumlinson, James H

Plants respond to insect-inflicted injury by systemically releasing relatively large amounts of several volatile compounds, mostly terpenoids and indole. As a result, the plants become highly attractive to natural enemies of the herbivorous insects. In maize, this systemic response can be induced by the uptake via the stem of an elicitor present in the oral secretions of caterpillars. Such an elicitor was isolated from the regurgitant of Spodoptera exigua larvae, identified as N-(17-hydroxylinolenoyl)-L-glutamine, and named volicitin. Here we present details on the procedure that was used to isolate volicitin and the biosasays that demonstrate its potency as an elicitor of maize volatiles that attract parasitoids. With a series of liquid chromatography purification steps, volicitin was separated from all other inactive substances in the regurgitant of larvae of the noctuid moth S. exigua. Maize seedlings that were incubated in very low concentrations of pure natural volicitin released relatively large amounts of terpenoids and became highly attractive to the parasitoid Microplitis croceipes. The identification of this and other insect-derived elicitors should allow us to determine their precise source and function, and better understand the evolutionary history of the phenomenon of herbivore-induced volatile emissions in plants.

1994, Turlings, Ted, Loughrin, John H, McCall, Philip J, Rose, Ursula S R, Lewis, W Joe, Tumlinson, James H

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.

1993, Tumlinson, James H, Turlings, Ted, Lewis, W Joe

Chemical cues enable female parasitic wasps to locate the eggs, larvae, or other life stages of the insects in or on which they place their eggs. These chemical signals, or semiochemicals, may be produced by the hosts and/or by the plants on which the hosts feed. The composition of the chemical signal often differs with different species of hosts or with different plants. New evidence suggests that the wasps exploit semiochemicals emitted by plants in response to insect herbivore feeding. The wasps learn to respond to the different blends of chemicals that indicate the location of their hosts and they can be trained to respond to a specific odor blend. Thus, it may be possible to increase their effectiveness for biological control by conditioning them, prior to their release, to search for a target pest in a particular crop.

1992, Turlings, Ted, Tumlinson, James H

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 margin-iventris; 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.

1997, Alborn, Hans, Turlings, Ted, Jones, Tappey, Stenhagen, G, Loughrin, John H, Tumlinson, James H

The compound N-(17-hydroxylinolenoyl)-L-glutamine (named here volicitin) was isolated from oral secretions of beet armyworm caterpillars. When applied to damaged leaves of corn seedlings, volicitin induces the seedlings to emit volatile compounds that attract parasitic wasps, natural enemies of the caterpillars. Mechanical damage of the leaves, without application of this compound, did not trigger release of the same blend of volatiles. Volicitin is a key component in a chain of chemical signals and biochemical processes that regulate tritrophic interactions among plants, insect herbivores, and natural enemies of the herbivores.

1994, McCall, Philip J, Turlings, Ted, Loughrin, John H, Proveaux, Adron T, Tumlinson, James H

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 com 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)-beta-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.

1993, McCall, Philip J, Turlings, Ted, Lewis, W Joe, Tumlinson, James H

A study was conducted to determine the primary source of volatile cues within the plant-host complex used by host-seeking free-flying female Microplitis croceipes Cresson in flight tunnel bioassays. In single-source and two-choice tests, using wasps given an oviposition experience on either cotton (Gossypium hirsutum) or cowpea (Vigna unguiculata) seedlings damaged by com earworm (CEW; Helicoverpa zea Boddie), the damaged seedlings were significantly more attractive than the CEW frass, which was in turn more attractive than the larvae themselves. In a series of two-choice wind-tunnel tests, the discriminatory ability of the wasps was examined, following various oviposition experiences. Significantly more wasps flew to plants with ''old '' damage than to plants with ''fresh '' damage, regardless of whether they had experience on fresh or old damage. In a comparison of plant species, wasps with only one experience on either host-damaged cotton or host-damaged cowpea were unable to distinguish between them, and showed no preference for either plant, whereas wasps with multiple experiences on a particular plant preferentially flew to that plant in the choice test. In comparing hosts with nonhosts, wasps successfully learned to distinguish CEW from beet armyworm (BAW, Spodoptera exigua) on cotton but were unable to distinguish CEW from either BAW or cabbage looper (Trichoplusia ni) on cowpea. The results show the important role played by plant volatiles in the location of hosts by M. croceipes and indicate the wasps' limitations in discriminating criminating among the various odors. The ecological advantages and disadvantages of this behavior are discussed.

1994, Loughrin, John H, Manukian, Ara, Heath, Robert R, Turlings, Ted, Tumlinson, James H

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.

1994, Stowe, Mark K, Turlings, Ted, Loughrin, John H, Lewis, W Joe, Tumlinson, James H

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.

1992, Tumlinson, James H, Turlings, Ted, Lewis, W Joe