Behavioral response ofTrichogramma pretiosum riley andTelenomus sphingis (Ashmead) to trichome/methyl ketone mediated resistance in tomato

Effects of methyl ketone (2-tridecanone and 2-undecanone)/glandular trichome-based resistance to insects ofLycopersicon hirsutum f.glabratum C.H. Mull, PI 134417, on the behavioral responses ofTrichogramma pretiosum Riley andTelenomus sphingis (Ashmead) were observed in the laboratory. ForT. pretiosum, these effects included (1) longer time required by the wasps to cross a leaf disk (diam. 16.3 mm), (2) higher percentage of wasps initiating flight from disks before reaching the edge, and (3) entrapment of wasps in trichome exudates. In tomato genotypes with varying densities of type VI glandular trichomes (3.1–9.2/mm²) but with no methyl ketones in the trichome tips, no such adverse effects were observed. The time taken to cross a disk or initiate flight byT. sphingis, a larger wasp thanT. pretiosum, was not significantly affected on 16.3-mm leaf disks, although the percentage ofT. sphingis initiating flight was directly correlated with trichome density among lines with no ketones. When placed on whole leaflets of plant lines with or without methyl ketones,T. sphingis was entangled by trichome exudates. However, unlikeT. pretiosum, T. sphingis was eventually able to free itself from entanglement. Landing rates byT. sphingis on PI 134417 foliage contained in dialysis tubes were also reduced. Data indicate that suppression of egg parasitism byT. sphingis on resistant foliage is due to both repellent action of its foliar volatiles and reduced searching rates by the parasitoids. Results indicate that a significant portion of the reduction of egg parasitism byT. pretiosum andT. sphingis is attributable to the effects of 2-tridecanone and/or 2-undecanone present in the tips of type VI glandular trichomes on PI 134417 foliage, although the trichomes also adversely affect the wasps even in plant lines without ketones.     

Toxicity of allelochemicals from wild insect-resistant tomatoLycopersicon hirsutum f.glabratum toCampoletis sonorensis,a parasitoid ofHeliothis zea

Greenhouse-grown plants of five tomato lines varying in their level of 2-tridecanone-mediated resistance toManduca sexta (L.) andLeptinotarsa decemlineata (Say) were found to adversely affect larvae ofCampoletis sonorensis (Cameron), a larval endoparasitoid ofHeliothis zea (Boddie), in a manner directly related to their level of resistance. The parasitoid larvae, which emerge as fifth instars from their host and construct a cocoon on the foliage of their hosts' host plant, suffered extensive mortality during cocoon spinning on highly resistant foliage. Mortality was greatest (82%) on the highly resistant plants ofLycopersicon hirsutum f.glabratum (accession PI 134417) and an F₁ backcross [(L. esculentum × PI 134417) × PI 134417] selection. Mortality was intermediate (40 and 28%, respectively) on backcross selections with moderate and low levels of resistance and least (8%) on susceptibleL. esculentum. Removal of the glandular trichomes, which contain 2-tridecanone in their tips, from the foliage eliminated differences in parasitoid mortality among plant lines.Bioassays of 2-tridecanone indicated that it is acutely toxic to fifth instarC. sonorensis larvae at the quantities associated with highly resistant foliage and produces symptoms identical to those observed on resistant foliage. 2-Undecanone, a second methyl ketone present in the glandular trichomes of resistant foliage, was also toxic toC. sonorensis larvae, but significantly less so than 2-tridecanone. The results support the hypothesis that 2-tridecanone is responsible for the observed mortality ofC. sonorensis larvae during cocoon construction on resistant foliage.     

Mortality and inhibition ofHelicoverpa zea Egg parasitism rates byTrichogramma in relation to trichome/methyl ketone-mediated insect resistance ofLycopersicon hirsutum f. glabratum,accession PI 134417

The glandular trichome/methyl ketone-mediated insect resistance of the wild tomato,Lycopersicon hirsutum f. glabratum C.H. Mull, accession PI 134417, toManduca sexta (L.) andLeptinotarsa decemlineata (Say) was shown to affect adverselyTrichogramma pretiosum Riley. AdultT. pretiosum were killed by direct contact with PI 134417 foliage and by exposure to its volatiles. This effect was greatly reduced or eliminated by removing the exudate of the glandular trichomes from the foliage. 2-Tridecanone, a principal consituent of the foliar glandular trichomes of PI 134417, was toxic to adultT. pretiosum at concentrations similar to those associated with PI 134417 foliage. Incubation of parasitizedHelicoverpa (=Heliothis) zea (Boddie) eggs on PI 134417 foliage or 2-tridecanone-treated filter paper significantly reduced the proportion of eggs producing adult parasitoids. Similarly, incubation of parasitizedH. zea eggs on filter paper treated with 2-undecanone, another constituent of the glandular trichomes of PI 134417, caused an increase in the percentage of host eggs containing dead parasitoid pupae.     

Effect of day length and light intensity on 2-tridecanone levels and resistance inLycopersicon hirsutum f.glabratum toManduca sexta

First instarManduca sexta (L.) larvae confined on foliage fromLycopersicon hirsutum f.glabratum (accession PI 134417) plants grown under a long-day regime exhibited greater mortality than larvae on foliage from plants grown under a short-day regime. 2-Tridecanone, a toxin important in the insect resistance of PI 134417, was significantly more abundant in the foliage of plants grown under the long-than the short-day regimes. Light intensity influenced neither 2-tridecanone levels nor the expression of resistance. The density of glandular trichomes, which secrete 2-tridecanone, was influenced by an interaction between day length and light intensity.Lepidoptera: Sphingidae.Paper no. 6503 of the Journal Series of the North Carolina Agricultural Research Service, Raleigh, North Carolina 27650.     

Activity of volatile compounds in glandular trichomes ofLycopersicon species against two insect herbivores

Several major chemicals in the glandular heads of type VI trichomes ofLycopersicon species were identified and quantified by gas chromatography and mass spectrometry. Two normal odd-chained ketones, 2-undecanone (47 ng) and 2-tridecanone (146 ng), and one unknown sesquiterpene (5 ng), comprised approximately 95% of the contents of a gland ofL.hirsutum f.glabratum Mull. In a closely related plant,L.hirsutum Humb. & Bonpl. (LA 361), two unknown insecticidal sesquiterpenes accounted for 6% of the gland contents. Additionally, small amounts of one unknown monoterpene and another unknown sesquiterpene were found in type VI glands of a commercial tomato variety,L.esculentum Mill. Bioassays comparing the gland exudate (by direct contact) and isooctane extracts of glands to neonate larvae ofKeiferia lycopersicella (Walsingham) (Lepidoptera: Gelechiidae) andSpodoptera exigua (Hübner) (Lepidoptera: Noctuidae) indicated that: (1) 2-tridecanone and 2-undecanone were the major insecticidal compounds inL.hirsutum f.glabratum, (2) the two unknown sesquiterpenes inL.hirsutum were acutely toxic to both species, and (3) gland contents in the commercial tomato variety provided only a physical barrier toK.lycopersicella, and were not detrimental toS.exigua. In topical bioassay trials, synthetic mixtures of 2-tridecanone and 2-undecanone (3 1) demonstrated potentiation. Concentrations of these chemicals decreased as trichomes aged. Quantities of insecticidal chemicals and density of type VI trichomes varied with plant age and location within plants.     

Inhibition ofCampoletis sonorensis parasitism ofHeliothis zea and of parasitoid development by 2-tridecanone-mediated insect resistance of wild tomato

Field populations ofHeliothis spp. were sampled for levels of naturally occurring larval parasitism on six tomato lines varying in levels of 2-tridecanone-mediated resistance toManduca sexta (L.) andLeptinotarsa decemlineata (Say). Second and third instars were parasitized byCampoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae) andCotesia (=Apantales)marginiventris (Cresson) (Hymenoptera: Braconidae) in 1984 through 1986 and byMicropletis croceipes (Cresson) (Hymenoptera: Braconidae) in 1986. Differences in parasitism by individual and multiple species among host plants were not demonstrated. However, levels of parasitism were low and variable among replicates. Total larval parasitism averaged across all plant lines was less than 6% in 1984 and 1986 and approximately 11% in 1985. In laboratory cage studies,C. sonorensis parasitized fewerH. zea larvae on tomato foliage with high levels of 2-tridecanone than on foliage with low levels. RearingH. zea on diet containing 2-tridecanone and 2-undecanone did not alter incidence of parasitism byC, sonorensis; nor did rearing parasitizedH. zea larvae on chemically treated host diets precondition the parasitoid to higher or lower mortality when transferred to foliage as a substrate for cocoon spinning, regardless of the foliage genotype. However, parasitoid survival during cocoon spinning on foliage varied significantly among plant lines in a manner corresponding to the level of 2-tridecanone-mediated resistance of the foliage. Parasitoid mortality was greatest on highly resistant foliage and lowest on susceptible foliage.     

Ester and ketone components of aggregation pheromone ofDrosophila hydei (Diptera: Drosophilidae)

Existence of an aggregation pheromone inDrosophila hydei was demonstrated by laboratory bioassay. The pheromone was produced by mature males, but both sexes responded. The nonpolar components consisted of three esters: the methyl, ethyl, and 1-methylethyl (isopropyl) esters of 2-methyl-(E)-2 butenoic (tiglic) acid, and two ketones: 2-tridecanone and 2-pentadecanone. The ketones and esters alone were only minimally active in the laboratory bioassay, but 2-tridecanone was highly synergistic with each of the esters, mixtures attracting 3–60 times more flies than the single components. 2-Pentadecanone was less active, but it did cause significant increases in activity when added to synthetic mixtures. The nonpolar portion of an extract of mature males and an equivalent mixture of the synthetic components were not significantly different in bioassay. Neither the esters nor the ketones were detected in sexually immature males or in females of any age. In extracts of mature males, ethyl tiglate was usually the most abundant ester component, with a mean of 8 ± 5 (SD) ng/male. The absolute and relative levels of the other esters were more variable. The mean level of methyl ketones in the extracts was 122 ± 106 (SD) ng/male, of which 85–93% was 2-tridecanone.     

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.     

Potential uses of kairomones for behavioral manipulation ofCotesia marginiventris (Cresson)

The effects of kairomone pattern and preconditioning on parasitization rates of fall armyworm larvae,Spodoptera frugiperda (J.E. Smith) byCotesia (=Apanteles)marginiventris (Cresson) were investigated in the laboratory and greenhouse using a hexane extract of frass and actual fall armyworm frass. Parasitization rates increased 55 and 26% in Petri dishes and on corn seedlings, respectively, when the entire experimental area was sprayed with the frass extract. Applying the extract in spots resulted in a 20–30% reduction in parasitization compared to treating the entire area. However, spot application produced significantly better parasitization rates compared to the control treatment. Exposing the parasitoids to actual fall armyworm frass resulted in ca. 50% greater retention in the release area and an increase of ca. 60–75% in the number of parasitoids searching.C. marginiventris parasitized factitious hosts topically treated with an extract of fall armyworm frass.Mention of a commercial or proprietary product does not constitute an endorsement by the USDA.Submitted in partial fulfillment of the requirements for the degree Doctor of Philosophy, Department of Entomology and Nematology, University of Florida, Gainesville     

Herbivore-Induced Plant Volatiles Mediate In-Flight Host Discrimination by Parasitoids

Herbivore feeding induces plants to emit volatiles that are detectable and reliable cues for foraging parasitoids, which allows them to perform oriented host searching. We investigated whether these plant volatiles play a role in avoiding parasitoid competition by discriminating parasitized from unparasitized hosts in flight. In a wind tunnel set-up, we used mechanically damaged plants treated with regurgitant containing elicitors to simulate and standardize herbivore feeding. The solitary parasitoid Cotesia rubecula discriminated among volatile blends from Brussels sprouts plants treated with regurgitant of unparasitized Pieris rapae or P. brassicae caterpillars over blends emitted by plants treated with regurgitant of parasitized caterpillars. The gregarious Cotesia glomerata discriminated between volatiles induced by regurgitant from parasitized and unparasitized caterpillars of its major host species, P. brassicae. Gas chromatography-mass spectrometry analysis of headspace odors revealed that cabbage plants treated with regurgitant of parasitized P. brassicae caterpillars emitted lower amounts of volatiles than plants treated with unparasitized caterpillars. We demonstrate (1) that parasitoids can detect, in flight, whether their hosts contain competitors, and (2) that plants reduce the production of specific herbivore-induced volatiles after a successful recruitment of their bodyguards. As the induced volatiles bear biosynthetic and ecological costs to plants, downregulation of their production has adaptive value. These findings add a new level of intricacy to plant–parasitoid interactions.     

(Z)-10-Heptadecen-2-one and other 2-ketones in the aggregation pheromone blend ofDrosophila martensis,D. buzzatii,andD. serido

(Z)-10-Heptadecen-2-one was identified as the major aggregation pheromone component inDrosophila martensis, D. buzzatii, andD. serido. Aliphatic 2-ketones were not detected in newly eclosed males or in virgin females of any age. The amount of (Z)-10-heptadecen-2-one in the ejaculatory bulb and on the cuticle of males increased with age. Only trace quantities of (Z)-10-heptadecen-2-one were transferred to the female during mating. 2-Tridecanone was found in the ejaculatory bulb and on the cuticle of maleD. martensis andD. buzzatii, but notD. serido. The amount of 2-tridecanone increased with age. Unexpectedly,2-tridecanone inhibited the aggregation activity of (Z)-10-heptadecen-2-one inD. buzzatii. InD. martensis, 2-tridecanone was significantly less attractive than controls but did not decrease the attractiveness of one fly equivalent of (Z)-10-heptadecen-2-one.D. serido males did not have any 2-tridecanone and the activity of (Z)-10-heptadecen-2-one was not diminished inD. serido by the presence of 2-tridecanone.     

Volatile ketones from interdigital glands of black-tailed deer,Odocileus hemionus columbianus

Three volatile ketones, 2-tridecanone, (E)-3-tridecen-2-one and (E)-4-tridecen-2-one were identified in interdigital gland extracts from black-tailed deer,Odocoileus hemionus columbianus. The major compound, (E)-3-tridecen-2-one, inhibited the growth of several species of fungi and grampositive bacteria. The bacterium,Propionibacterium acnes, and the fungus,Trichophyton mentagrophytes required a minimum concentration (MIC) of 12.5 µg/ml and 25 µg/ml, respectively, for inhibition, (E)-3-Tridecen-2-one represents a new class of lipid antibiotics found on animal skin. The second major compound is this secretion, 2-tridecanone, was not active against any of the organisms tested.     

Toxicity studies of analogs of 2-tridecanone,a naturally occurring toxicant from a wild tomato

Toxicity bioassays of the naturally occurring insecticide 2-tridecanone and a group of structural analogs against the tomato fruitworm (Heliothis zea) reveal a significant influence of chain length on toxicity of methyl ketones. This effect may be due to the differential ability of these compounds to penetrate lipid barriers and reach the active site, since a close relationship is seen between toxicity and lipophilicity. Congeners of chain lenths 15 and over are less active than predicted by this relationship, possibly due to steric effects.Received for publication June 29, 1981, paper no. 6973 of the Journal Series of the North Carolina Agricultural Research Service, Raleigh, North Carolina 27650.     

Sequestration ofVeratrum alkaloids by specialistRhadinoceraea nodicornis konow (Hymenoptera,Tenthredinidae) and its ecoethological implications

The larvae of the specialist sawflyRhadinoceraea nodicornis Konow (Hymenoptera, Tenthredinidae) store in their hemolymph ceveratrum alkaloids originating from the host plantVeratrum album L. (Liliales, Melanthiaceae). The major alkaloid found in the hemolymph is 3-acetyl-zygadenine. Qualitative and quantitative data showed that the plant alkaloid 3-angeloylzygadenine is most probably metabolized in the larval gut to zygadenine and then acetylated. A still unidentified alkaloid with a molecular weight of 591 Da was detected in plant leaves as well as in the gut, hemolymph, and excrement of larvae. Protoveratrine A and B, on the other hand, seem to be degraded by the larvae. These findings indicate that the pathway of ceveratrum alkaloids inR. nodicornis larvae is fourfold: direct sequestration, metabolism followed by sequestration, excretion of intact alkaloids, and degradation. In contrast, no ceveratrum alkaloids were detected in the hemolymph and excrement of larvae of the generalist sawflyAglaostigma sp. fed withV. album leaves. Bioassays with the antMyrmica rubra L. proved that the hemolymph ofR. nodicornis larvae is highly deterrent and toxic. In bioassays evaluating defensive efficiency against predators (ants, spiders, and bushcrickets), no larvae were eaten. Ceveratrum alkaloids were also detected in the hibernating prepupae ofR. nodicornis. In feeding bioassays, the shrewCrocidura russula Hermann rarely fed upon prepupae, suggesting that this stage is also protected from predation to some degree. In field surveys, the only parasitoids recorded were two ichneumonid species that are believed to be specialized onR. nodicornis. Bioassays and field observations enable us to suppose thatR. nodicornis and its enemies produce a food web of ion connectance.     

Behavioral and growth responses of specialist herbivore,Homoeosoma electellum,to major terpenoid of its host,Helianthus SPP

The responses of a sunflower specialist,Homoeosoma electellum, the sunflower moth, to the terpenoids produced by its host plant,Helianthus, were measured. Larvae were reared on synthetic diet containing one of three concentrations of the dominant sesquiterpene lactone found in glandular trichomes ofH. maximilliani. Treatments were initiated at each of three larval ages. Pupal weight was significantly reduced, but the effect diminished as the larvae aged. Survival and development time were unaffected by various treatments. In behavioral tests, larvae showed no preference for untreated synthetic diet compared to diet containing the secondary compound at a concentration of 1% by dry weight. When the concentration was raised to 5%, all but last-instar larvae showed a significant preference for the untreated diet. A second behavioral test measured the damage done to whole florets and an array of floral parts offered to larvae of different ages. The damage pattern of floral tissues changed as the larvae grew older, demonstrating that the willingness of larvae to eat tissues contaminated with trichome contents increased with age. The value of the glandular trichome contents as a defense againstH. electellum is discussed.     

Contact stimulants fromHeliothis virescens that influence the behavior of females of the tachinid,Eucelatoria bryani

Factors acting at contact or close range affected the behavior associated with host seeking of females, but not of males, of the tachinid,Eucelatoria bryani Sabrosky. Females were arrested by components of larvae ofHeliothis virescens (F.) and by a dichloromethane extract of okra leaves. A hexane extract ofH. virescens frass and a chloroform-methanol extract ofH. virescens larvae were both active. In addition to chemicals, shape and size were involved because females were arrested by small inert objects the size ofH. virescens larvae and frass.In cooperation with the Louisiana Agricultural Experiment Station and the Texas Agricultural Experiment Station.Mention of a proprietary product does not constitute an endorsement by the USDA.     

Olfactory Responses of Parasitoid Apoanagyrus lopezi to Odor of Plants, Mealybugs, and Plant–Mealybug Complexes

Apoanagyrus (Epidinocarsis) lopezi De Santis is an endoparasitoid used in the biological control of the cassava mealybug Phenacoccus manihoti Matile-Ferrero in Africa. The response of naive and mated females of A. lopezi to odors from cassava plant (var. Zanaga), parasitized or unparasitized mealybugs, and plant–mealybug host complexes with or without feeding hosts was investigated in a Y-tube olfactometer. Dual-choice tests revealed that mealybug-infested plants and mealybug-damaged plants were the major sources of volatiles that attract female parasitoids to the microhabitat of its hosts. The emission of volatile chemicals appears not to be limited to the infested plant part but to occur systemically throughout the plant. On their own, unparasitized mealybugs were more attractive than uninfested plants or parasitized mealybugs alone. Parasitization of P. manihoti by A. lopezi decreased the response of parasitoids to mealybugs or mealybug–plant complexes. Plants infested with unparasitized hosts attracted more female parasitoids than plants infested with parasitized mealybugs. These results indicate that, in the long-range host-searching process, females of A. lopezi respond mainly to mealybug-induced synomones, and specific host-derived cues play a minor role.     

Role of plant volatiles in the search for a host by parasitoidDiglyphus isaea (Hymenoptera: Eulophidae)

Diglyphus isaea Walker is a larval ectoparasitoid used in biological pest control against the American serpentine leaf minerLiriomyza trifolii Burgess. We studied the parasitoid's host searching behavior, using olfactometric methods. Our data show that the parasitoids locate host larvae (a leafmining dipteran) on the basis of volatile signals released by the plant-host complex. FemaleD. isaea are strongly attracted to the odors arising from damaged bean plants, whereas they show practically no response to intact plants. The results of our chemical analyses showed that about 15 components were present, two of which,cis-3-hexen-1-ol and 4-hydroxy-4-methyl-2-pentanone, were present in significantly larger quantities in the leaf extracts from mined or damaged bean plants than in those from healthy plants. The damage inflicted by the host larvae on these plants triggers the release of larger amounts of these substances, which probably lead the parasites to their hosts. The compounds thus act as synomones.     

A neolignoid feeding deterrent againstLuehdorfia puziloi larvae (lepidoptera: Papilionidae) fromHeterotropa aspera,a host plant of sibling species,L. japonica

A feeding deterrent against larvae of a papilionid butterfly,Luehdorfia puziloi (Parnassiinae), a specialist onAsiasarum plants (Aristolochiaceae), was isolated from another aristolochiaceous plant,Heterotropa aspera. Antifeedant activity was exhibited by then-hexane-soluble fraction that proved to contain at least two active components. One of the deterrents was identified as a neolignan compound, asatone. The concentration of asatone inH. aspera was estimated at approximately 225 ppm, and larval feeding ofL. puziloi was significantly deterred at concentrations over 90 ppm. By contrast, asatone was not detectable (< 1 ppm, if any) in its host plant,Asiasarum sieboldii.     

Kairomone strains of Euclytiaflava (Townsend), a parasitoid of stink bugs

Tachinid flies commonly use the pheromones and allomones of stink bugs (Pentatomidae) as host-finding kairomones. Pheromone-baited traps for predaceous (Podisus spp.) and phytophagous (Euschistus spp.) pentatomids were used to obtain tachinid parasitoids in order to study the semiochemical relationships between these parasitic flies and their stink bug hosts. Gas chromatography–electroantennogram detector (GC-EAD) experiments and field tests were conducted to determine if pheromone strains of the tachinids, Euclytia flava and Hemyda aurata, occur in nature and to determine if the EAD-active compound, (E)-2-octenal (a common allomone compound of Heteroptera), affects attraction of tachinid parasitoids to synthetic Podisus pheromones. Addition of (E)-2-octenal to Podisus spp. synthetic pheromones in field traps tended to suppress attraction of the bugs, whereas (E)-2-octenal decreased, did not affect, or increased pheromonal attraction of tachinid parasitoids depending on the host species pheromone being tested and the habitat type in which the traps were deployed. Evidence from GC-EAD experiments of E. flava associated with different stink bug hosts suggested that kairomone-strains of this tachinid parasitoid coexist naturally. The significance of cryptic kairomone strains of parasitoids for classical biological control is disc ussed, and the mechanisms whereby parasitoids evolve kairomonally mediated host-shifts is considered.