Orientation behavior and effect of experience and laboratory rearing on responses ofCotesia melanoscela (Ratzeburg) (Hymenoptera: Braconidae) to gypsy moth silk kairomone

Cotesia melanoscela responds the same way to the silk of its host, gypsy moth larvae,Lymantria dispar L., whether or not it has previously been exposed to hosts. Parasites maintained in the laboratory for six or 25 generations also responded similarly, suggesting that orientation behavior is not modified by laboratory rearing. Details of silk-related orientation behavior were analyzed by tracing paths of female parasites when on or off silk-covered substrates. Females made 31 ° average turns every 0.5 cm whether or not they were examining silk. They tended to turn back onto a silked area when encountering a border, and their speed of movement when not examining silk was about three times higher than when examining silk.     

Plant-natural enemy association in tritrophic system,Cotesia rubecula-Pieris rapae-brassicaceae (Cruciferae). III: Collection and identification of plant and frass volatiles

To elucidate the identity of the volatile compounds that could be involved in the searching behavior of the parasitoidCotesia rubecula Marshall (Hymenoptera: Braconidae), the volatiles released by cabbage and frass of Lepidoptera feeding on cabbage were collected and analyzed using a gas chromatograph-mass spectrometer. The volatiles emitted by intact cabbage were -pinene, -pinene, myrcene, 1,8-cineole,n-hexyl acetate,cis-3-hexen-1-yl acetate, and dimethyl trisulfide. Mechanical damage on an intact plant induced the release of two more compounds,trans-2-hexenal and 1-methoxy-3-methylene-2-pentanone. Current feeding by larvae ofPieris rapae L. (Pieridae) induced the plant to release all the compounds released after mechanical damage and additionally 4-methyl-3-pentenal and allyl isothiocyanate. Current feeding by larvae ofPlutella xylostella L. (Plutellidae) induced the plant to release all the compounds present after mechanical damage and additionally allyl isothiocyanate. The volatiles emitted after feeding by the lepidopterans had ceased were the same as those emitted by cabbage damaged by mechanical means. The blend of volatiles emitted by frass was comprised of plant chemicals, mainly sulfur compounds. Frass ofP. rapae emitted allyl isothiocyanate, methyl isothiocyanate, methyl propyl sulfide, dimethyl trisulfide,S-methyl methane thiosulfinate, 4-methyl-3-pentenal,trans-2-hexenal, and 2,3-dihydro-4-methyl furan. Frass ofP. xylostella emitted only dimethyl trisulfide andS-methyl methane thiosulfinate. The blend of volatiles emitted by frass is herbivore-species specific.     

Plant-natural enemy association in the tritrophic systemCotesia rubecula-Pieris rapae-brassicaceae (cruciferae): II. Preference ofC. rubecula for landing and searching

The responses of the parasitoidCotesia rubecula to differently damaged cabbages were recorded during a series of choice tests. To determine if flyingC. rubecula can discriminate differences in the blend of volatiles emitted by cabbages damaged by different causes and how plant volatiles released from a distant source affect the searching behavior ofC. rubecula once searching on a plant, wasps were presented with a choice of plants located one behind the other and separated by a distance of 15 cm. The sources of damage were: cabbage damaged by the host (Pieris rapae), by a nonhost lepidopteran herbivore (Plutella xylostella), by a nonhost, noninsect herbivore (snail), and by mechanical means. The results showed that the site of first landing and the time spent searching on the leaves was influenced by the type of damage inflicted on plants. Wasps preferred to land on cabbages damaged by host and nonhost species of Lepidoptera over those damaged by snails and mechanical means. No preference was observed for first landing between cabbages damaged by the two species of Lepidoptera or between cabbages damaged by snails and mechanical means. Cabbage damaged byP. rapae was searched most intensively, followed by cabbage damaged byP. xylostella, cabbage damaged by snails, and cabbage damaged by mechanical means.C. rubecula differentiates between the volatile blends emitted by differently damaged cabbages, and it is attracted to volatiles related to recent lepidopteran damage. Wasps searched longer on freshly damaged than on leaves with older damage.     

Role of diet in host selection ofHeliothis virescens by parasitoidCampoletis sonorensis (Hymenoptera: Ichneumonidae)

Gas chromatographic analysis revealed that chemicals attractive toCampoletis sonorensis (Cameron), previously identified in cotton, were not present in wheat germ diet-rearedHeliothis virescens (F.) larvae. Diet-reared larvae fed cotton obtained the chemicals from cotton, with the consequence of enhanced kairomonal activity of the larvae and their frass toC. sonorensis. Parasitoids, presented a choice between cotton, cotton plus hosts, hosts alone, and control in an olfactometer, responded non-randomly, with the greatest number of responses to cotton plus hosts, and three times as many responses to cotton alone as to larvae alone. The role of the plant in the parasitoid-host relationship is discussed.     

Volatile infochemicals used in host and host habitat location byCotesia flavipes Cameron andCotesia sesamiae (Cameron) (Hymenoptera: Braconidae), larval parasitoids of stemborers on graminae

FemaleCotesia flavipes Cameron andCotesia sesamiae (Cameron) were attracted to odors in a Y-tube olfactometer from uninfested maize (Zea mays L.), sorghum [Sorghum bicolor (L.)], and napier grass (Pennisetum purpureum Schumach). In dual choice tests,Cotesia flavipes showed a preference for maize over sorghum, while maize and napier grass were equally attractive. In contrast,Cotesia sesamiae preferred volatiles from sorghum and napier grass over those from maize. The two parasitoids were significantly more attracted to maize infested with the stemborers,Chilo partellus (Swinhoe),Chilo orichalcociliellus Strand,Sesamia calamistis Hampson, andBusseola fusca (Fuller), than uninfested maize. In dual choice tests,Cotesia flavipes andCotesia sesamiae were unable to discriminate between odors from plants infested by the different species of stemborers.     

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.     

Ovipositional behavior ofbracon mellitor say (Hymenoptera: Braconidae), a parasitoid of boll weevil (anthonomus grandis Boh.)

FemaleBracon mellitor Say responded to the frass of dietreared boll weevil larvae by probing with the ovipositor. Similar responses were elicited by the hexane and chloroform-methanol fractions after differential extraction of boll weevil feces. The active component of the chloroform-methanol fraction was identified as methylp-hydroxybenzoate (methyl parasept). Because the methyl parasept is an artificial component of the diet, the results suggest that the parasitoid response may be associatively learned. The response to methyl parasept decreased with time in the absence of reinforcement. Results demonstrate that certain chemicals may release behavior normally evoked by kairomones, and may interfere with the isolation of natural kairomones.This paper was approved for publication as TA 12350 by the Director, Texas Agricultural Experiment Station. This study was conducted in cooperation with the USDA. It was supported, in part, by the National Science Foundation and the International Biological Program (NSF-SC-0030) of the University of California. The findings are those of the authors, and not necessarily those of the University of California or the National Science Foundation. Mention of a proprietary or commercial product in this paper does not constitute an endorsement of this product by the USDA.     

Orientation ofMicroplitis croceipes (Hymenoptera: Braconidae) to green leaf volatiles: Dose-response curves

FemaleMicroplitis croceipes wasps were tested in a wind tunnel for their ability to orient to various concentrations of eight different green leaf volatile (GLV) substances [hexanal, (E)-2-hexenal, (E)-2-hexen-1-ol, (Z)-3-hexen-1-ol, (E)-2-hexenyl acetate, (Z)-3-hexenyl acetate, (Z)-3-hexenyl propionate, and (Z)-3-hexenyl butyrate]. Overall, the esters elicited the greatest percentage of successful orientation flights, the alcohols elicited an intermediate response, and the aldehydes elicited a low response. The semilog dose-response curves were generally hill-shaped with high responses at medium release rates and low responses at high or low release rates. For the aldehydes, positive responses occurred at all GLV release rates between 0.01 and 100 nl/min. For some alcohols and esters, positive responses occurred at release rates as low as 1 pl/min and as high as 1μl/min. These data show thatM. croceipes wasps are strongly attracted to GLVs and are capable of orienting to GLV concentrations that would occur in nature when a caterpillar feeds on a green leaf. Hence, in nature, GLVs may be important clues, enablingM. croceipes to locate their hosts.     

Beneficial arthropod behavior mediated by airborne semiochemicals. II. Olfactometric studies of host location by the parasitoidMicroplitis croceipes (Cresson) (Hymenoptera: Braconidae)

The response ofMicroplitis croceipes (Cresson) to odors from a plant-host complex was investigated using a four-choice olfactometer. Female, but not male, parasitoids responded in a dose-dependent fashion to volatiles from the plant-host complex and oviposition experience enhanced this response. Female age had no apparent effect on the response. Both artificially damaged leaves and frass elicited positive responses but of lower magnitude than those elicited by the plant-host complex. Volatiles collected from the plant-host complex placed on filter paper also elicited positive responses by female parasitoids.Mention of a commercial or proprietary product does not constitute an endorsement by the USDA.     

Sources of fall armyworm,Spodoptera frugiperda (Lepidoptera: Noctuidae), kairomones eliciting host-finding behavior inCotesia (=Apanteles) marginivenitris (Hymenoptera: Braconidae)

Bioassay responses inCotesia marginiventris (Cresson) females to materials derived from fall armyworm (FAW) larvae,Spodoptera frugiperda (J. E. Smith), were most intense for frass and somewhat less intense for larval and pupal cutical materials, scales, exuviae, silk, and oral secretion, with FAW larval hemolymph eliciting only a slight response. The highest percentage of ovipositor probing was caused by frass (100%) and moth scales (90%). Various types of corn-leaf damage when assayed alone did not produce responses as intense as when assayed in combination with frass, cuticle material, and oral secretion. Parasitoid response was somewhat better to frass derived from FAW larvae feeding on corn and peanut leaves than from larvae feeding on the foliage of soybeans, Bermuda grass, cowpeas, or laboratory diet. Hexane and chloroform were better than methanol and water for extracting active material from FAW frass, and chloroform was the best of these solvents for extracting corn leaves. Serial dilutions of frass extracts resulted in a reduction in parasitoid response.This paper was submitted in partial fulfillment of the requirements for Doctor of Philosophy, Department of Entomology and Nematology, University of Florida, Gainesville.     

Effects of comsumption of high and low nicotine tobacco byManduca sexta (Lepidoptera: Sphingidae) on survival of gregarious endoparasitoidCotesia congregata (Hymenoptera: Braconidae)

The significance of nicotine in the three trophic level interaction involving tobacco (Nicotiana tabacum), the tobacco hornworm (Manduca sexta), and the parasitoidCotesia congregata was investigated in field plots of two varieties of tobacco which had about a 10-fold difference in their nicotine content. WhileM. sexta mortality, rates of parasitism byC. congregata, and the total number ofC. congregata larvae produced per host were similar on each of the two varieties, the number of parasitoids reaching adult-hood on the low nicotine treatment was nearly twice that on the high nicotine treatment. This difference was due to the significantly greater proportion of parasitoid larvae which failed to emerge from the host or that died prior to pupation after emerging from hosts which fed on the high nicotine variety. A greater proportion of larvae from hosts which fed on the low nicotine tobacco died as pupae. No treatment differences occurred for either sex of the parasitoid in individual dry weight, longevity, or pupal development time, except that female pupal duration was prolonged in the high nicotine treatment. These results support the suggestion that plant allelochemicals, which may function to provide plant resistance against pest herbivores, can be detrimental to natural enemies of the pest.Scientific article No. A4148 of the Maryland Agricultural Experiment Station, Department of Entomology. Research supported by NSF grant BSR-84-00614.     

Source of sex pheromone of the egg-larval parasitoid,Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae)

A sex pheromone ofAscogaster reticulatus Watanabe (Hymenoptera: Braconidae), identified as (Z)-9-hexadecenal, elicits males' antennal matesearching behavior. In order to localize the source of sex pheromone production, each body part was separated and extracted with hexane and then subjected to 9-cm Petri dish bioassay. The highest activity was found in thorax extract. Among legs, wings, and thorax, legs have the highest activity. Among fore, middle, and hind legs, hind legs have the highest activity. Among coxa and trochanter, femur, tibia, and tarsus, tibia has the highest activity. From these results, the presence of a tibial sex pheromone gland was suggested.     

Plant-natural enemy association in the tritrophic system,Cotesia rubecula-Pieris rapae-brassiceae (cruciferae): I. Sources of infochemicals

The role of airborne infochemicals in host selection by the parasitoidCotesia rubecula (Marshal) (Hymenoptera: Braconidae) was examined in a wind tunnel. To elucidate the role of volatile chemicals in attractingC. rubecula to cabbage infested by the host [Pieris rapae L. (Lepidoptera: Pieridae)], the potential sources of volatiles related toP. rapae infestation on cabbage were tested individually. The responses of females to nonhost plant species, bean and geranium, as well as to frass of a nonhost lepidopteran were also examined.C. rubecula was attracted to cabbage previously infested byP. rapae and to frass and regurgitate ofP. rapae. No attraction was observed to larvae ofP. rapae alone. Females were also attracted to mechanically damaged cabbage, cabbage previously infested byPlutella xylostella L. (Lepidoptera: Plutellidae) (a nonhost lepidopteran herbivore), and cabbage previously infested by snails (a nonhost, noninsect herbivore). Intact cabbage, bean, and geranium plants elicited no attraction. A low frequency of attraction was observed to mechanically damaged bean and geranium. Attraction was also observed to frass ofP. xylostella. Volatiles from cabbage related to damage, and volatiles from frass and regurgitate of the host seem to play an important role in guidingC. rubecula to plants infested by its host.     

Plant allelochemicals and insect parasitoids effects of nicotine onCotesia congregata (say) (Hymenoptera: Braconidae) andHyposoter annulipes (Cresson) (Hymenoptera: Ichneumonidae)

Parasitoids developing within tobacco hornworms or fall army-worms exhibit significant differences in development and survival depending on whether their hosts fed on nicotine-free or nicotine-containing diets. The effects of nicotine were more severe on the relatively less adapted parasitoid,H. annulipes than the specialist parasitoid,Cotesia congregata. Labeled alkaloid originally placed in herbivore diet was incorporated in several parasitoid tissues. These results suggest that interactions between plant allelochemicals and parasitoids should be considered in the development of theory on insect herbivory and plant defense.Scientific article No. A4408, Contrib. No. 7397 of the Maryland Agricultural Experiment Station, Department of Entomology. Research supported by USDA. Competitive Grant No. 59-2241-1-1-749-0 and NSF grant BSR-84-00614.Mention of a commercial product does not constitute an endorsement.     

Effect of kairomones from egg and female adult stages ofOstrinia nubilalis (Hübner) (Lepidoptera,Pyralidae) onTrichogramma brassicae Bezdenko (Hymenoptera,Trichogrammatidae) female kinesis

Volatile chemicals emanating from the different developmental stages ofOstrinia nubilalis Hübner (Lepidoptera, Pyralidae) increase the mobility ofTrichogramma brassicae Bezdenko (Hymenoptera, Trichogrammatidae) in a linear airflow olfactometer. In this paper, we have demonstrated that airborne chemicals from egg masses and virgin females during calling activity stimulate an intensive search behavior byTrichogramma females. On the other hand, emanations from mated females with extruded abdominal tips do not incite the parasitoid's movement. For the moment we cannot elucidate, with these bioassays, the real role of these kairomones as attractants, guides, stimulants, or retainers.     

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.     

Mating and oviposition byCotesia (=Apanteles) marginiventris (Hymenoptera: Braconidae) in presence of synthetic pheromone ofSpodoptera frugiperda (Lepidoptera: Noctuidae)

Two blends of fall armyworm,Spodoptera frugiperda (J.E. Smith), pheromonal components were evaluated in the laboratory for possible close-range effects on mating and oviposition byCotesia marginiventris (Cresson). Neither a two- nor a five-component blend had any significant effect on mating or parasitization ofS. frugiperda larvae by this parasitoid. Dosages of 200, 400, and 800 g were tested.     

Kairomonal activities of 2-acylcyclohexane-1,3 diones produced byEphestia kuehniella zeller in eliciting searching behavior by the parasitoidBracon hebetor (say)

2-Acylcyclohexane-1,3-diones produced in the mandibular glands ofEphestia kuehniella Zeller (Lepidoptera: Pyralidae) fifth instars acted as arrestment and host-trail following kairomones for the parasitoid,Bracon hebetor (Say) (Hymenoptera: Braconidae). The behavioral response of the parasitoids to the kairomone varied with kairomone concentration and distribution. However, only small differences in activity were noted for the different mandibular gland components.B. hebetor females that encountered filter paper patches impregnated with the kairomone exhibited antennation and probing behavior. Females followed trails formed with 2-[(Z,E)12,14-hexadecadienoyl]cyclohexane-1,3-dione in the same manner exhibited with host-made trails. At concentrations of 1.0 g/mm and above, trail following was interrupted by frequent probing.     

Host microhabitat location by stem-borer parasitoidCotesia flavipes: the role of herbivore volatiles and locally and systemically induced plant volatiles

The origin of olfactory stimuli involved in the host microhabitat location inCotesia flavipes, a parasitoid of stem-borer larvae, was investigated in a Y-tube olfactometer. The response of femaleC. flavipes towards different components of the plant-host complex, consisting of a maize plant infested with two or more larvae of the stem borerChilo partellus, was tested in dualchoice tests. The concealed lifestyle of the stem-borer larvae did not limit the emission of volatiles attractive to a parasitoid. A major source of the attractive volatiles from the plant-host complex was the stem-borer-injured stem, including the frass produced by the feeding larvae. Moreover, the production of volatiles attractive to a parasitoid was not restricted to the infested stem part but occurs systemically throughout the plant. The uninfested leaves of a stem-borer-infested plant were found to emit volatiles that attract femaleC. flavipes. We further demonstrate that an exogenous elicitor of this systemic plant response is situated in the regurgitate of a stem-borer larva. When a minor amount of regurgitate is inoculated into the stem of an uninfested plant, the leaves of the treated plant emit volatiles that attract femaleC. flavipes.     

Role of host-produced stimuli and learning in host selection behavior ofCotesia (=Apanteles) marginiventris (Cresson)

The study was conducted to determine how various factors, including learning, influence the host-selection behavior of the larval parasitoid Cotesia (=Apanteles)marginiventris (Cresson). Frass, silk, and feeding damage fromSpodoptera frugiperda (J.E. Smith) larvae elicited visits and antennal examinations by females of the parasitoid. Learning played a role in the effective response to these stimuli in that previous contact experience with hosts and/or chewed leaves, exuviae, frass, or hemolymph significantly enhanced the response of the parasitoid. Previous contact with host plants alone did not improve the responses. Experienced parasitoids were more active and spent less time at rest than inexperienced parasitoids. Previous experience was also found to be of significant importance in the ability of the parasitoid to discriminate between parasitized and unparasitized host larvae.Hymenoptera: Braconidae.In cooperation with the University of Georgia College of Agriculture Experiment Stations, Coastal Plain Station, Tifton, Georgia 31793-0748.Mention of a proprietary product in this paper does not constitute endorsement of this product by the USDA.Visiting scientist with the Department of Entomology, Coastal Plain Station, Tifton, Georgia, during this study.