Influence of life history differences of two tachinid parasitoids ofHelicoverpa zea (Boddie) (Lepidoptera: Noctuidae) on their interactions with glandular trichome/methyl ketone-based insect resistance in tomato

The effects of glandular trichome/methyl ketone (2-tridecanone and 2-undecanone) -based insect resistance in the wild tomato,Lycopersicon hirsutum f.glabratum C.H. Mull, accession PI 134417, onArchytas marmoratus (Townsend) andEucelatoria bryani (Sabrosky) (Diptera: Tachinidae), both parasitoids ofHelicoverpa (=Heliothis)zea (Boddie) (Lepidoptera: Noctuidae), were investigated in the laboratory.A. marmoratus deposits larvae (planidia) on the foliage of its host's food plant; planidia attach to passing hosts, penetrate the cuticle, and develop in the host pupae.E. bryani larviposits directly into its host; its larvae develop in the host larva.A. marmoratus planidia are killed by glandular trichomes of PI 134417 and also by trichomes of hybrid lines with no methyl ketones. The methyl ketones are toxic to planidia, but at least part of the effect is due to other factors, possibly physical entanglement. Both species can be affected indirectly by methyl ketones in the diet of the host. 2-Undecanone reduces the percentage ofA. marmoratus larvae that reach pupation. This effect is evidently due to premature death and desiccation of the host pupa caused by 2-undecanone. 2-Tridecanone in host diets had no effect onA. marmoratus. InE. bryani, 2-tridecanone in the diet of the host reduced the number of parasitoids yielded by each parasitized host, although not the overall percentage of hosts parasitized. 2-Undecanone in the diet of the host had no effect onE. bryani.We thank M. Woodall for typing; V.B. Covington, D. Bumgarner, and B. O'Brien for technical assistance; L.A. Jones for assistance with gas chromatography; P.H. Adler for supplyingE. bryani puparia to initiate colony; and Drs. F. Gould, G.C. Rock, and M. Barbercheck for comments.     

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.     

Behavior ofHeliothis virescens (F.) in presence of oviposition deterrents from elderberry

Extracts prepared from elderberry,Sambucus simpsonii Rehd., leaves with either acetone, dichloromethane, distilled water, ethanol, hexane, or methanol deterred oviposition byHeliothis virescens (F.) on treated substrates in the laboratory. Doses of the aqueous extract equivalent to as little as 0.8 mg of leaves/cm2 of oviposition substrate were effective in reducing egg deposition. There was no significant difference in the mean number of landings on extract-treated and untreated surfaces. When either the antennae, proboscis, or the metathoracic legs were removed from female moths, there was no significant effect on oviposition on paper towels treated with elderberry leaf-water extract in laboratory bioassays, but in field cages, moths without these appendages deposited significantly fewer eggs on treated leaves of tobacco plants, a preferred host. There was no evidence that elderberry leaf-water extract affected mating byH. virescens.Lepidoptera: Noctuidae.Mention of a commercial or proprietary product does not constitute an endorsement by the USDA.     

Identification and bioassay of kairomones forHelicoverpa zea

Hexane extracts of leaves of 307 accessions from 73 host plant species ofHelicoverpa zea were analyzed by gas chromatography (GC) and used forH. zea oviposition and neonate larvae orientation bioassays. The gas chromatographic (GC) retention times of compounds statistically associated with behavioral activity were identified by correlation of GC peak area with oviposition and larval orientation preferences. Although taxonomically diverse in their origin, compounds for study were purified from extracts of species of the genusLycopersicon, due to their relative abundance. The structures of eight long-chain alkanes associated with oviposition preference were assigned by mass spectrometry, and the structures of five similarly associated organic acids and a terpenoid alkene were identified by¹H and¹³C nuclear magnetic resonance spectroscopy. The structures of a number of other phytochemicals from the plant leaves were identified for comparative purposes, including a previously unknown terpene, 7-epizingiberene. Bioassays were performed on the isolated acids and on the alkane wax fractions of severalLycopersicon species, and significant differences were found in oviposition stimulation for both classes of compounds. Of the hundreds of compounds found in the extracts, none were observed to act as oviposition deterrents. The results of these bioassays may be useful in explaining the broad host range ofH. zea, as well as the process and evolution of host plant selection for oviposition.     

Structure-activity relationships for analogs of (+)-(E)-endo-Β-bergamoten-12-oic acid,an oviposition stimulant ofHelicoverpa zea (Boddie)

-Bergamotenoic acid, a compound previously shown to stimulate oviposition inH. zea, was converted into a set of bicyclic analogs and tested with a set of acyclic side chain analogs to ascertain the molecular structure that maximizes insect behavioral response. While changes in the bicyclic ring elicited no variation in response, alteration in the side chain structure of-bergamotenoic acid resulted in significant changes in moth preference. Free rotation about the C-C bond proximal to the carboxylic acid group appears to be an important structural factor, since saturation of the side chain double bond significantly increased activity. The carboxylic acid group seems to be required for strong oviposition stimulation, since analogs lacking the carboxylic acid group exhibited no significant oviposition activity. Oviposition preference ofH. zea was also influenced by the length of the hydrocarbon chain to which the carboxylic acid is attached. While hexanoic acid was found inactive, the ovipositional preference for the heptanoic and octanoic acids was greatest for the one 8-carbon tested. This and other work suggest that carboxylic acids of specific chain lengths influence the oviposition behavior of bothHelicoverpa andHeliothis species and may be associated with host-plant selection. The potential use of this information in designing integrated pest management strategies for control ofH. zea is discussed.     

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.     

Comparison of sex pheromone composition and pheromone-mediated male behavior of laboratory-reared and wildHeliothis zea (Lepidoptera: Noctuidae)

Analysis of ovipositor extracts of lab-reared (> 120 generations) and wildHeliothis zea indicated small but significant differences in the percent composition of the four aldehyde components of the sex pheromone. (Z)-11-hexadecen-1-ol (Z11–16OH) was present in both populations and amounted to only 2.8% of the total pheromone. There was no significant difference in four of the six behavioral categories between lab-reared and wild males exposed to the four-component sex pheromone in the flight tunnel. Ninety and 84% males flew to the pheromone source, respectively. However, with the addition ofZ11–16OH to the pheromone blend, none of the wild males flew upwind to the stimulus source, whereas 36% of the lab-reared males completed the flight. It is suggested that prolonged inbreeding in closed quarters rendered these males less discriminating to qualitative differences in a pheromone blend.     

Attraction ofHeliothis virescens (F.) (Lepidoptera: Noctuidae) to volatiles from extracts of cotton flowers

Mated and virgin female and virgin male tobacco budworm moths,Heliothis virescens (F.), responded via directed upwind flight in wind-tunnel bioassays to volatiles from floral extracts of cotton,Gossypium hirsutum L. Significantly more male and female moths landed on cloth dispensers treated with a methylene chloride extract of debracted flowers than on control dispensers treated only with methylene chloride. Only mated females landed in significant numbers on the dispensers treated with extract of cotton squares, flowers (including bracts), or flower petals. After landing, most of the moths examined the dispensers by probing with their antennae, proboscis, and/or ovipositor.     

Kairomones and their use for management of entomophagous insects VIII. Effect of diet on the kairomonal activity of frass fromHeliothis zea (Boddie) larvae forMicroplitis croceipes (Cresson)

Heliothis zea (Boddie) larvae were reared on fresh plant material (cowpea cotyledons) or on an artificial laboratory diet. Effect of these two diets on the kairomonal activity of the frass and cuticle from the larvae, as well as the kairomonal activity of the diets themselves, forMicroplitis croceipes (Cresson) was determined. Diet was found to significantly affect the kairomonal activity of the frass although the diets themselves were not active.Lepidoptera: Noctuidae.Hymenoptera: Braconidae.Part of the work reported here was done as a high school science project. This project was awarded the Grand Award in Life Sciences at the 29th and 30th Georgia Science and Engineering Fair, April 1977 and 1978, respectively; the Fourth Place Award in Zoology at the International Science and Engineering Fair held in Cleveland, Ohio, May 1977; the Second Place Award in Zoology at the International Science and Engineering Fair held in Anaheim, California, May 1978; and received other special awards.In cooperation with the University of Georgia College of Agriculture Experiment Stations, Coastal Plain Station, Tifton, Georgia 31794.Mention of a commercial or proprietary product in this paper does not constitute endorsement by the USDA.     

Influence ofHeliothis virescens sex pheromone dispensers on captures ofH. zea males in pheromone traps relative to distance and wind direction

Evaluations conducted by placingHeliothis virescens (F.) sex pheromone (virelure) dispensers at different distances in the predominant downwind and upwind directions fromHeliothis zea (Boddie) pheromone traps indicated that reductions inH. zea male captures were greatest relative to distance when theH. zea traps were located downwind from the virelure dispensers than when the traps were located upwind. When operating traps for both species at the same site, the influence of virelure dispensers on captures inH. zea pheromone traps would be minimized by placing theH. zea traps upwind of theH. virescens traps and, if wind direction is variable, the traps should be spaced at least 75 m apart.Lepidoptera: Noctuidae.In cooperation with the Texas Agricultural Experiment Station, Texas A&M University, College Station, Texas 77843. This paper reports the results of research only. Mention of a commercial or proprietary product in this paper does not constitute an endorsement of this product by USDA.     

Behavioral responses of maleHeliothis zea moths in sustained-flight tunnel to combinations of 4 compounds identified from female sex pheromone gland

Each of the four compounds that have been identified from sex pheromone glands ofHeliothis zea female moths was examined for its ability to elicit sexual responses from male moths in a flight tunnel. Males flew upwind to (Z)-11-hexadecenal alone, but greater levels of behavioral activity were evoked with the addition of (Z)-9-hexadecenal to the treatment. Addition of hexadecanal or (Z)-7-hexadecenal to the initial two components had no effect in raising the behavioral response of the males in the flight tunnel whether added singularly at both the normal gland-emission ratio or at varying ratios or in combination at the normal ratio. Live, calling females elicited levels of sexual activity from males not significantly different from that elicited by the mixture of (Z)-11- and (Z)-9-hexadecenal on cotton wicks.Lepidoptera: Noctuidae.     

Compound interactions effects of plant antioxidants in combination with carbaryl on performance ofTrichoplusia ni (Cabbage Looper)

Plant chemicals naturally exist in complex mixtures, which can interact either additively, synergistically, or antagonistically. We investigated the potential interactions of three naturally occurring antioxidants— nordihydroguaiaretic acid (NDGA), safrole, and -tocopherol—with the general insecticide carbarayl to affect the performance of cabbage looper larvae (Trichoplusia ni). The cabbage looper is known to produce a mixed-function oxidase enzyme system in response to the presence of carbaryl. We proposed that plant antioxidants would interfere with enzymatic oxidation, enhancing the susceptibility of this insect to carbaryl. Insects were fed artificial diets containing each antioxidant alone or in pairwise combinations with the insecticide carbaryl to test for their effects on the insect's nutritional measurement indices. The three antioxidants tested were not equally effective individually against insect survivorship and interacted differentially in combination with the insecticide. The nutritional indices were measured on insects fed diets containing the chemicals at nonlethal doses. Insects fed 0.001 % wet wt NDGA diets grew 1.62 times less, and had gross and net conversion efficiencies reduced 3.20 and 3.63 times, respectively, compared to the control larvae. Carbaryl (0.002% wet wt) in combination with NDGA acts as an antagonist to the effects mentioned above, while safrole (1 × 10^–4 wet wt) had an additive effect when combined with the insecticide, reducing 1.76 times larval relative growth rate and efficiency of conversion of ingested food in respect to the control. The larvae fed significantly more (1.2 times) on both insecticide and safrole diets than on the controls or their combined diets. Larvae fed -tocopherol alone or in combination with carbaryl had similar growth and conversion efficiencies as controls. We conclude that the effects of different combinations of compounds cannot be predicted a priori and must be determined experimentally.Operated for the U.S. Department of Energy by the University of California under Contract No. DE-ACO3-76-SF00012. This article was supported by the Center for Intermedia Transport Research (EPA Contract CR-81172-01) and by the Ecological Research Division of the Office of Health and Environmental Research, U.S. Department of Energy.     

Beneficial arthropod behavior mediated by airborne semiochemicals. IX. Differential response ofTrichogramma pretiosum,an egg parasitoid ofHeliothis zea,to various olfactory cues

The behavior ofTrichogramma pretiosum Nixon wasps when exposed to different olfactory cues was studied in a wind tunnel. Compared to clean air, the sex pheromone of its hostHeliothis zea (Boddie) increased wasp residence times, walking times, and path lengths on a platform and decreased walking velocity. If wasps were released on top of a glass rod above a platform, the odor caused the wasps to land shortly after takeoff. In addition, a clear dose effect with regard to total residence and walking times was found. These responses were not elicited by three dosages of the sex pheromone ofSpodoptera frugiperda (J.E. Smith) or by a blend of saturated acetates. These results correspond with the observation thatH. zea is a common field host ofT. pretiosum, whereas eggs ofS. frugiperda are rarely attacked by this parasitoid.     

Influence ofAmaranthus hybridus L. allelochemics on oviposition behavior ofSpodoptera exigua andS. eridania (Lepidoptera: Noctuidae)

Common pigweed,Amaranthus hybridus L., is a favorite host of the beet army worm (BAW),Spodoptera exigua L. Chemicals extracted from homogenized pigweed with distilled water, ethanol, or dichloromethane and sprayed back on pigweed deterred oviposition by the BAW. Similarly, water extracts of frass from conspecific larvae or southern armyworm (SAW) larvae,S. eridania (Cramer), fed pigweed leaves and sprayed back on pigweed plants also deterred BAW oviposition, thus confirming that deterrence was due to plant allelochemics rather than specific compounds associated with the metabolic or excretory products of the larvae. Confirmation of the presence of oviposition-deterring chemicals in pigweed was used to explain a previously observed seasonal displacement of BAW by SAW on pigweed in the field.Mention of a commercial or proprietary product does not constitute an endorsement by the USDA.     

Effects of cotton condensed tannin,maysin (Corn) and pinitol (soybeans) onHeliothis zea growth and development

Maysin, a flavone glycoside from corn silks, inhibits ingestion, and thus growth, ofHeliothis zea (Boddie) larvae. Pinitol from soybeans inhibitedH. zea growth by the same mechanism. Despite the widely held assumption that tannins inhibit growth by inhibiting assimilation, cotton condensed tannin inhibitedH. zea growth by reducing ingestion; no evidence was found for a reduction in assimilation. Neonate larvae are shown to be much more sensitive to allelochemics than larvae that have fed on control diet before being transferred to diet containing plant allelochemics.Reference to a company and/or product named by the department is only for purposes of information and does not imply approval or recommendation of the product to the exclusion of others which may also be suitable.Published with the approval of the director of the Delaware Agricultural Experiment Station as Miscellaneous Paper No. 968, Contribution No. 514 of the Department of Entomology and Applied Ecology, University of Delaware, Newark, Delaware 19711.     

Heliothis subflexa (Gn.) (Lepidoptera: Noctuidae): Demonstration of oviposition stimulant from groundcherry using novel bioassay

Methanol extracts of homogenized groundcherry,Physalis angulata, leaves increased egg deposition byHeliothis subflexa (Gn.) (HS) on treated tobacco plants (a nonhost) 8.5-fold over untreated controls. In doseresponse tests using whole-leaf washes of groundcherry leaves, the threshold of positive response vs. no response to the chemical stimulant was within one log dose unit when compared to the controls. This response was consistent whether the chemical was evaluated on plants in greenhouse-cage tests or in an olfactometer using pieces of broadcloth as the oviposition substrate. The olfactometer used allows year-round study of the behavioral effects of plant allelochemics on insect oviposition behavior in a controlled environment.This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or the recommendation of its use by USDA.     

Selection of a polyethylene tubing formulation of (Z)-9-tetradecen-1-ol formate and its use in disrupting pheromone communication inHeliothis zea (Boddie)

The release rates of (Z)-9-tetradecen-1-ol formate (Z9TDF) from four sizes of polyethylene tubing were measured periodically for 50 days by collecting the Z9TDF vapors on a polymeric adsorbent. The resulting release rate curves had shapes that were determined by the tubing's diameter and wall thickness. One tubing size that combined good longevity with adequately high release rates was tested in the field to determine whether it could disrupt pheromone communication of the corn earworm,Heliothis zea (Boddie). We observed a low percentage of disruption, but release rate measurements made concurrently showed that the tubing was releasing Z9TDF normally. In a second field test, a larger quantity of Z9TDF was released, and 87% disruption was attained for 66 days.Mention of a commercial or proprietary product in this paper does not constitute endorsement of that product by the USDA.     

Pheromone hydrolysis by cuticular and interior esterases of the antennae,legs, and wings of the cabbage looper moth,Trichoplusia ni (Hübner)

Examination was made of the hydrolytic activities of esterases obtained from the antennae, legs, and wings of 3-day-old cabbage looper moths,Trichoplusia ni (Hübner), by elution and by homogenation of those appendages. Pheromone hydrolysis in 1-min assays was monitored by use of tritium-labeled (Z)-7-dodecen-1-ol acetate and thin-layer chromatography to separate the reaction products. Listed according to the activities of the esterases obtained by homogenation, the organs were antennae > legs > wings. In contrast, the order according to the activities of the eluted esterases was wings > legs > antennae. Also, the eluted enzymes were less active than the esterases obtained by homogenization. The relatively high pheromone-hydrolyzing activity present in homogenized antennae suggests that the esterases originated inside the antennae and lends support to the hypothesis proposed in earlier investigations that pheromone-inactivating enzymes may play an important role in the olfactory process, possibly by clearing pheromone from the vicinity of the olfactory receptors. The esterases detected on the cuticle, on the other hand, may function by preventing surface accumulation of pheromone. The higher measured esterase activity in homogenates of prothoracic legs than of mesothoracic or metathoracic legs suggests that the prothoracic legs, which are used to clean the antennae of debris, may function by removing and degrading pheromone from the surface of antennae.Mention of a commercial or proprietary product does not constitute an endorsement by the USDA.     

Effects of host plant,Gossypium hirsutum L., on sexual attraction of cabbage looper moths,Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae)

Unmated female or male cabbage looper moths,Trichoplusia ni (Hübner), were attracted more often in a flight tunnel to a cage with moths of the opposite sex and a bouquet of cotton foliage. Increased sexual attractiveness of females with plants may be a result of stimulation of pheromone release in response to plant odor, since more males were attracted when odor of cotton foliage was passed over females than when odor of females was passed over cotton foliage before venting into the flight tunnel. Increased sexual attractiveness of males with plants is due in part to host odor enhancement of female attraction to male pheromone, since more females were attracted to synthetic male pheromone (a blend of enantiomers of linalool and isomers of cresol) and a cotton leaf extract than were attracted to male pheromone alone. A short synthesis procedure was developed for (S)-(+)-linalool, the major component of the male sex pheromone, isolated from hair pencils, used in these tests.     

Growth inhibitors in tomato (Lycopersicon) to tomato fruitworm (Heliothis zea)

Several compounds that retard the larval growth of the tomato fruitworm,Heliothis zea (Boddie) have been isolated and identified from tomato leaves,Lycopersicon esculentum Mill. The major allelochemics are -tomatine (I), chlorogenic acid (II), rutin (III), and a new caffeyl derivative of an aldaric acid (IV). The isolation, analyses, and toxicity of these compounds toH. zea are presented.Reference to a company and/or product named by the department is only for purposes of information and does not imply approval or recommendation of the product to the exclusion of others which may also be suitable