Turlings, Ted

2004, Degen, Thomas, Dillmann, Christine, Marion-Poll, Frédéric, Turlings, Ted

Maize plants (Zea mays) attacked by caterpillars release a mixture of odorous compounds that attract parasitic wasps, natural enemies of the herbivores. We assessed the genetic variability of these induced volatile emissions among 31 maize inbred lines representing a broad range of genetic diversity used by breeders in Europe and North America. Odors were collected from young plants that had been induced by injecting them with caterpillar regurgitant. Significant variation among lines was found for all 23 volatile compounds included in the analysis: the lines differed enormously in the total amount of volatiles emitted and showed highly variable odor profiles distinctive of each genotype. Principal component analysis performed on the relative quantities of particular compounds within the blend revealed clusters of highly correlated volatiles, which may share common metabolic pathways. European and American lines belonging to established heterotic groups were loosely separated from each other, with the most clear-cut difference in the typical release of (E)-beta-caryophyllene by European lines. There was no correlation between the distances among the lines based on their odor profiles and their respective genetic distances previously assessed by neutral RFLP markers. This most comprehensive study to date on intraspecific variation in induced odor emission by maize plants provides a further example of the remarkably high genetic diversity conserved within this important crop plant. A better understanding of the genetic control of induced odor emissions may help in the development of maize varieties particularly attractive to parasitoids and other biological control agents and perhaps more repellent for herbivores.

1996, Boeve, Jean-Luc, Lengwiler, Urs, Tollsten, Lars, Dorn, Silvia, Turlings, Ted

The effect of infestation by larvae of the European apple sawfly (Hoplocampa testudinea) on the emission of volatiles from apple fruitlets was investigated. Healthy apples emitted a blend of terpenoids and a few aromatic and short aliphatic compounds. Infested apples emitted the same compounds as healthy apples. However, trans,trans-alpha-farnesene, trans-beta-ocimene and another terpenoid were emitted in significantly larger amounts, whereas the other volatiles showed no quantitative change. The results were obtained with picked apples and could be confirmed in the field with single apples left on the tree. Several non-terpenoid volatiles emanated from the frass and from epidermal glands of the sawfly larvae. The possible ecological significance of the increased emission of terpenoids by infested apples is discussed with reference to a parasitic wasp that attacks the sawfly larvae.

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.

2003, Gouinguene, Sandrine, Alborn, Hans, Turlings, Ted

Maize plants under attack by caterpillars emit a specific blend of volatiles that is highly attractive to parasitic wasps. The release of these signals is induced by elicitors in the caterpillar regurgitant. Studies suggest that plants respond differently to different herbivore species and even to different herbivore stages, thus providing parasitoids and predators with specific signals. We tested if this is the case for different larval instars of the noctuid moth Spodoptera littoralis when they feed on maize plants. Cut maize plants were incubated in diluted regurgitant from second, third, or fifth instar caterpillars. There were no differences in total amount released after these treatments, but there were small differences in the release of the minor compounds phenethyl acetate and alpha-humulene. Regurgitant of all three instars contained the elicitor volicitin. To test the effect of actual feeding by the larvae, potted plants were infested with caterpillars of one of the three instars, and volatiles were collected the following day. The intensity of the emissions was correlated with the number of larvae feeding on a plant, and with the amount of damage inflicted, but was independent of the instar that caused the damage. We also used artificial damage to mimic the manner of feeding of each instar to test the importance of physical aspects of damages for the odor emission. The emission was highly variable, but no differences were found among the different types of damage. In olfactometer tests, Microplitis rufiventris, a parasitoid that can only successfully parasitize second and early third instar S. littoralis, did not differentiate among the odors of maize plants attacked by different instar larvae. The odor analyses as well as the parasitoid's responses indicate that maize odors induced by S. littoralis provide parasitoids with poor information on the larval developmental stage. We discuss the results in the context of variability and lack of specificity in odorous plant signals.

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.

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.

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.