W. J. Lewis

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.

Herbivore-infested plants selectively attract parasitoids

In response to insect herbivory, plants synthesize and emit blends of volatile compounds from their damaged and undamaged tissues, which act as important host-location cues for parasitic insects. Here we use chemical and behavioural assays to show that these plant emissions can transmit herbivore-specific information that is detectable by parasitic wasps (parasitoids). Tobacco, cotton and maize plants each produce distinct volatile blends in response to damage by two closely related herbivore species, Heliothis virescens and Helicoverpa zea. The specialist parasitic wasp Cardiochiles nigriceps exploits these differences to distinguish infestation by its host, H. virescens, from that by H.zea. The production by phylogenetically diverse plant species and the exploitation by parasitoids of highly specific chemical signals, keyed to individual herbivore species, indicates that the interaction between plants and the natural enemies of the herbivores that attack them is more sophisticated than previously realized.

Parasitoid Foraging and Learning

The diminutive size of most parasitoids undoubtedly has limited their choice as subjects for behavioral study, despite their great diversity in lifestyles and reproductive strategies. The present chapter addresses their foraging behavior as influenced by learning. Most of their adult life female parasitoids search for host insects which, in turn, are under selection to avoid being found and devoured. This scenario sets the stage for the evolution of diverse hide-and-seek games played by parasitoids and their victims, most often herbivores. That parasitoids are successful in their quest for hosts is evidenced by the vast number of parasitoid species and their importance in insect management.

Terminology of chemical releasing stimuli in intraspecific and interspecific interactions

The terminology of chemical releasing stimuli is examined in an attempt to reduce some apparent confusion. Two new classes of interspecific chemical signals, synomone and apneumone, are proposed.

Larval-damaged plants: source of volatile synomones that guide the parasitoid Cotesia marginiventris to the micro-habitat of its hosts

Single and dual choice tests in a flight tunnel revealed that plants damaged by host larvae are the main source of the volatiles that attract females of the parasitoid Cotesia marginiventris (Cresson) to the microhabitat of its hosts. Frass and host larvae, the other two major components of a complete plant‐host complex, were significantly less attractive than the damaged seedlings; frass alone was more attractive than larvae alone. However, a recombination of larvae with the damaged seedlings was significantly more attractive than the damaged leaves alone, or damaged leaves with frass. This was due to the additional feeding damage done by the larvae. The role of plants in the host‐finding behaviour of parasitoids is discussed.

Beneficial arthropod behavior mediated by airborne semiochemicals

Oriented responses ofMicroplitis croceipes (Cresson) to airborne odors of actively feedingHeliothis zea (Boddie) larvae were observed in a flight tunnel. The behavior ofM. croceipes prior to and during sustained, oriented flights was videotaped and analyzed in detail. Preflight exposure of the parasitoid to feces and other components of the plant-host complex were found to be vital in effective flight behavior, while maturation of the parasitoid had little effect. The increased frequency of oriented flight that resulted from preflight exposure of a plant-host complex persisted for at least 24 hr.

A variable-response model for parasitoid foraging behavior

An important factor inducing variability in foraging behavior in parasitic wasps is experience gained by the insect. Together with the insects genetic constitution and physiological state, experience ultimately defines the behavioral repertoire under specified environmental circumstances. We present a conceptual variable-response model based on several major observations of a foraging parasitoids responses to stimuli involved in the hostfinding process. These major observations are that (1) different stimuli evoke different responses or levels of response, (2) strong responses are less variable than weak ones, (3) learning can change response levels, (4) learning increases originally low responses more than originally high responses, and (5) hostderived stimuli serve as rewards in associative learning of other stimuli. The model specifies how the intrinsic variability of a response will depend on the magnitude of the response and predicts when and how learning will modify the insects behavior. Additional hypotheses related to the model concern how experience with a stimulus modifies behavioral responses to other stimuli, how animals respond in multistimulus situations, which stimuli act to reinforce behavioral responses to other stimuli in the learning process, and finally, how generalist and specialist species differ in their behavioral plasticity. We postulate that insight into behavioral variability in the foraging behavior of natural enemies may be a help, if not a prerequisite, for the efficient application of parasitoids in pest management.

Semiochemicals for use with parasitoids: Status and future.

Allelochemicals are known to serve important roles at all steps in the host-searching sequence of parasitoids. We discuss the various roles of these allelochemics and the type of information needed to develop their use in pest control, which to date has been very limited. Rapid advancements are being made with respect to airborne chemicals and longer-range foraging behavior. Moreover, recent discoveries have shown that genetic diversity in parasitoid populations and phenotypic plasticity of individuals, together with their physiological state, often result in substantial variations in the response to chemical cues. Successful application of semiochemical-parasitoid systems will require management of these intrinsic parasitoid variables as well as management of the foraging environment. We illustrate emerging technology for such an application. For the immediate future, the development of this technology will allow us to: (1) define the genetic and phenotypic foraging profiles important to consistent and efficient parasitoid foraging, and (2) establish the proper propagation and release procedures and monitoring bioassays necessary to ensure appropriate behavioral and physiological qualities of released organisms. For the long term, we envision technology for comprehensively manipulating the pest/crop environment in ways that would provide foraging stimuli and other needs important to retention and efficiency of parasitoids.

SPECIFICITY OF SYSTEMICALLY RELEASED COTTON VOLATILES AS ATTRACTANTS FOR SPECIALIST AND GENERALIST PARASITIC WASPS

Cotton plants under herbivore attack release volatile semiochemicals that attract natural enemies of the herbivores to the damaged plant. The volatiles released in response to herbivory are not only released from the damaged leaves but from the entire cotton plant. We found that cotton plants that released myrcene, (Z)-3-hexenyl acetate, (E)-β-ocimene, linalool, (E)-4,8-dimethyl-1,3,7-nonatriene, (E)-β-farnesene, and (E, E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene systemically from undamaged leaves of caterpillar damaged plants were attractive to the generalist parasitoid Cotesia marginiventris and the specialist parasitoid Microplitis croceipes. Plants from which the caterpillar damaged leaves were removed and that released those compounds systemically were significantly preferred over undamaged control plants in two-choice experiments in a flight tunnel. Artificially damaged cotton plants that released green leafy volatiles and constitutive terpenoids were less attractive for M. croceipes and C. marginiventris. Only C. marginiventris preferred artificially damaged plants over undamaged control plants, whereas M. croceipes showed no preference. The apparent lack of specificity of systemically released compounds in response to different herbivores feeding on the lower leaves is discussed.

Kairomones and their use for management of entomophagous insects : XIII. Kairomonal activity forTrichogramma spp. of abdominal tips, excretion, and a synthetic sex pheromone blend ofHeliothis zea (Boddie) moths.

Volatile chemicals emanating from an excretion (apparently meconium) and abdominal tips of femaleHeliothis zea (Boddie) moths mediated increased rates of parasitization ofH. zea eggs byTrichogramma pretiosum Riley. A blend of synthetic chemicals, consisting of hexadecanal, (Z)-7-hexadecenal, (Z)-9-hexadecenal, and (Z)-11-hexadecenal, which has been identified as the sex pheromone of and from the abdominal tip of femaleH. zea moths, also increased rates of parasitization ofH. zea eggs byT. pretiosum in greenhouse experiments. In addition, parasitization ofH. zea eggs by wildTrichogramma spp., in field plots of cotton,Gossypium hirsutum L., treated with a similar blend of chemicals, in Conrel fibers, was more than double that in untreated plots.