Onion fly and little house fly host finding selectively mediated by decomposing onion and microbial volatiles

Responses of onion flies,Hylemya antiqua (Meigen), to various synthetic onion and microbial volatiles as well as volatiles from microbial cultures and decomposing onions were tested to characterize the most effective host-finding stimuli. Of nine onion and microbial volatiles tested individually, only the known attractant,n-dipropyl disulfide, caught significant numbers of flies. However, a blend of these volatiles attracted more flies than any single chemical, includingn-dipropyl disulfide. In another experiment, agar plates inoculated with microorganisms from decomposing onions did not attract onion flies. However, cut onions inoculated with microorganisms and conditioned 4 days caught more onion flies than freshly cut onions andn-dipropyl disulfide. These results suggest that a blend of chemicals, rather than a single key chemical, is the more effective host-finding stimulus, and that microbial activity enhances the attractancy of a blend of onion volatiles. Large numbers ofFannia canicularis (L.), the little house fly, responded to the microbial cultures, demonstrating the existence of a potent attractant for this muscid.Diptera: Anthomyiidae.Diptera: Muscidae.Paper No. 9470 of the Michigan State University Agricultural Experiment Station. Received for publication May 23, 1980.     

Search for potent attractants of onion flies

Of various chopped vegetables tested,Allium spp. high in propyl-containing alkyl sulfides (e.g.,cepa group) caught the most onion flies in trapping tests in the field. Fly catches to chopped onion increased with bait quantity. Attractancy of chopped onion changed dramatically during aging in the field; catch increased over the first few days, peaked at ca. fivefold over fresh material by 3–5 days, and then declined sharply. This age-dependent increase in attraction was not seen for garlic (known to have antimicrobial properties) nor with chopped onion mixed with chopped garlic. These data suggested that attraction of onion flies to onions was strongly influenced by microbial activity associated with decomposing onions. The bacteriumKlebsiella pneumoniae was identified as a major colonizer of onions maximally attractive to onion flies. This increased attraction is not due to the previously reported microbially produced volatiles ethyl acetate and tetramethyl pyrazine.Diptera: Anthomyiidae.Paper No. 11047 of the Michigan State University Agricultural Experiment Station.     

Yeast and corn hydrolysates and other nutritious materials as attractants for onion and seed flies

The attractancy of enzymatic yeast hydrolysate, a corn hydrolysate, brewers' yeast, honey, ammonia,n-dipropyl disulfide, and several combinations of these treatments was tested in an onion field containing onion flies,Hylemya antiqua (Meigen) and seedcorn flies,H. platura (Meigen). Enzymatic yeast hydrolysate (concentrated powder) proved to be highly attractive to both fly species; females were more responsive than males. Brewers' yeast and corn hydrolysate were intermediately attractive, while all other treatments were only slightly or not at all attractive. Although no steps were taken to prolong release of volatiles, some of the nutritious materials remained highly attractive even after 11 days. The yeast products may, at certain times, be even more attractive than specific host volatiles. However, their activity was not constant over time and may be influenced by the stage of reproductive development of female flies.Diptera: AnthomyiidaePaper No. 9511 of the Michigan State University Agricultural Experiment Station.     

Influence of cage design on precision of tube-trap bioassay for attractants of the onion fly,Delia antiqua

Responses of onion flies,Delia antiqua, to known attractants were measured in the laboratory with a novel tube-trap bioassay. The relative numbers of flies caught in tube traps baited with enzymatic yeast hydrolysate, brewer's yeast, andn-dipropyl disulfide were similar to those obtained previously with cone traps in the field. Changing the shape of the bioassay cage from a cuboid to a cylinder decreased the experimental error obtained from analysis of variance, as did rotating the floor of the circular cage. This bioassay should be useful in evaluating attractants for other insects that orient along the substrate.Diptera: Anthomyiidae.Paper No. 11327 of the Michigan State University Agricultural Experiment Station. Received for publication June 8, 1984.     

Responses ton-dipropyl disulfide by ovipositing onion flies: Effects of concentration and site of release

Onion fly females,Delia antiqua (Diptera: Anthomyiidae) laid the most eggs on ovipositional dishes havingn-dipropyl disulfide (Pr₂S₂) release rates of 1–6 ng/sec from polyethylene capsules placed beneath a sand substrate. When dipropyl disulfide was released from the wax coating of surrogate foliage rather than from the substrate, ovipositing females again responded differentially to various concentrations, laying more eggs around stems containing 0.075 and 0.089 mg/stem. Factorial combinations of several concentrations released from surrogate foliage and substrate showed that releases from surrogate foliage stimulated four times more egg-laying than releases from the substrate. Females tended to lay more eggs around surrogate stems having Pr₂S₂ at the base rather than on the upper half of foliage. Observations of individual females performing preovipositional examining behaviors on Pr₂S₂-treated surrogate stems indicated that females tended to land on the upper portions of the foliage, but after landing, spent most of their time examining areas of soil and surrogate within 1 cm of the soil-surrogate foliage interface. Surrogate stems provide a realistic context for investigating effects of plant chemicals on host-acceptance behaviors.Journal article No. 12034 of the Michigan Agricultural Experiment Station.This work was supported by USDA Competitive Grant 5901-0410-9-0229-0.     

Cinnamyl derivatives and monoterpenoids as nonspecific ovipositional deterrents of the onion fly

Laboratory dose-response choice tests and discriminate-dosage bioassays revealed wide variation in the effectiveness of cinnamyl, cinnamoyl, monoterpene, and phenethyl alcohol derivatives as ovipositional deterrents toDelia antiqua (Meigen), the onion fly. (E)-Cinnamic acids were not detectably deterrent. When formulated in particles of polyethylene glycol, (E)-cinnamaldehyde had a BR₉₀ (concentration eliciting 90% deterrency) of 1.0% and (E)-4-methoxycinnamaldehyde had a BR₉₀ of 0.38%. Among nine monoterpenoids tested,p-cymene was inactive, citronellal had a BR₉₀ of 3.7%, and terpinene-4-ol had a BR₉₀ of 0.46%. Para-substituted phenethyl alcohols gave increasing deterrence in the order: –NO₂, CH₃O–, –Cl, –CH₃, –H. Wide varieties of structures were deterrent: C-8 to C-13, intermediate in polarity, and possessing either oxygen-containing or nitrile functional groups. The air concentration of (E)-cinnamaldehyde at its BR₉₀ was 1.7 ng/ml. This relatively high concentration, the diversity in deterrent structures, and the lack of differences in deterrency among positional and optical isomers suggest that ovipositional deterrency in onion flies is mediated by receptors broadly tuned for detecting phenylpropenoid, phenolic, monoterpenoid, and perhaps other classes of allelochemicals.     

Host selection byHylemya antiqua laboratory bioassay and methods of obtaining host volatiles

An oviposition bioassay for the onion maggot,Hylemya antiqua (Meigen), is described in which females, in response to volatile stimulants, oviposit through small apertures onto moistened filter paper. Onion volatiles that act as attractants and oviposition stimulants were captured in Porapak Q from air passed over chopped onions in glass chambers. Pentane extracts from odor-impregnated Porapak Q induced 30–50% of the oviposition that occurred in response to 15-g onion-slice stimuli. Extracts presented in pentane on waxed dental cotton wicks induced more constant oviposition over a 3-day period than extracts on unwaxed wicks. Extract of the Porapak Q-captured volatiles from bulbs of fresh, actively growing onions elicited a much stronger response than did stem and leaf extracts from the same onions. The bioassay techniques and chemical procedures developed in this study could be used in chemical isolation programs for host attractants or oviposition stimulants forH. antiqua or similar species.Diptera:Anthomyiidae.Research supported by National Research Council of Canada, Grant Nos. A3881 and A3706.     

Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L

When attacked by herbivorous insects, many plants emit volatile compounds that are used as cues by predators and parasitoids foraging for prey or hosts. While such interactions have been demonstrated in several host–plant complexes, in most studies, the herbivores involved are leaf-feeding arthropods. We studied the long-range plant volatiles involved in host location in a system based on a very different interaction since the herbivore is a fly whose larvae feed on the roots of cole plants in the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae). The parasitoid studied is Trybliographa rapae Westwood (Hymenoptera: Figitidae), a specialist larval endoparasitoid of D. radicum. Using a four-arm olfactometer, the attraction of naive T. rapae females toward uninfested and infested turnip plants was investigated. T. rapae females were not attracted to volatiles emanating from uninfested plants, whether presented as whole plants, roots, or leaves. In contrast, they were highly attracted to volatiles emitted by roots infested with D. radicum larvae, by undamaged parts of infested roots, and by undamaged leaves of infested plants. The production of parasitoid-attracting volatiles appeared to be systemic in this particular tritrophic system. The possible factors triggering this volatile emission were also investigated. Volatiles from leaves of water-stressed plants and artificially damaged plants were not attractive to T. rapae females, while volatiles emitted by leaves of artificially damaged plants treated with crushed D. radicum larvae were highly attractive. However, T. rapae females were not attracted to volatiles emitted by artificially damaged plants treated only with crushed salivary glands from D. radicum larvae. These results demonstrate the systemic production of herbivore-induced volatiles in this host-plant complex. Although the emission of parasitoid attracting volatiles is induced by factors present in the herbivorous host, their exact origin remains unclear. The probable nature of the volatiles involved and the possible origin of the elicitor of volatiles release are discussed.     

Stimulo-deterrent diversion: A concept and its possible application to onion maggot control

Considerable basic information has been gathered on the interaction between the onion fly (Delia antiqua) and its host plant, the onion (Allium cepa). An attempt is underway to manipulate ovipositional behavior of this pest by treating onion seedlings with chemical deterrents while simultaneously providing deeply planted onion culls on which onion flies prefer to lay. This bipolar strategy of behavioral manipulation, termed stimulo-deterrent diversion (SDD), has the advantages of: (1) avoiding severe pest deprival and concomitant overriding of deterrents, (2) combining the effects of push and pull multiplicatively, and (3) providing opportunities for enhanced biological control in sites where the pest becomes concentrated. The suggestion is made that using SDD along with soil insecticide might relax or even reverse selection for physiological resistance ofD. antiqua to insecticides. As tools of molecular biology open new possibilities for manipulating plants and their allelochemicals, applied chemical ecologists should consider arranging situations where the allelochemicals have clear and adaptive messages for the pest. By combining toxins and deterrents at sites where feeding should be prevented, while simultaneously expediting use of alternative plants or plant parts, it might be possible to guide pest evolution toward paths of less conflict with human interest.     

Host selection byHylemya antiqua (Meigen)

Volatile components ofAllium cepa L, trapped in and recovered from Porapak Q, were separated by gas-liquid and thin-layer chromatography. Fractions eliciting oviposition fromHylemya antiqua (Meigen) were analyzed by combined gas chromatography-mass spectroscopy (GC-MS) and were found to contain saturated and unsaturated disulfides. Authentic samples of the identified components were obtained by synthesis and tested for oviposition response byH.antiqua. Three new attractants and oviposition stimulants forH. antiqua are methyl propyl disulfide,cis-propenyl propyl disulfide, andtrans-propenyl propyl disulfide. All were present in greater proportion in the volatiles from fresh onions than from stored onions. Dimethyl disulfide, methylcis-propenyl disulfide, and methyltrans-propenyl disulfide did not elicit significant oviposition fromH. antiqua.Diptera: Anthomyiidae.Research supported by National Research Council of Canada, Operating Grant Nos. A3881 and A3706, and Cooperative Grant No. A0243: Nature Products Chemistry and Chemical Ecology of Canadian Insect and Disease Pests.     

Synthesis of the stereoisomers of the female sex pheromone of the Hessian fly,Mayetiola destructor

The female-produced sex pheromone of the Hessian fly,Mayetiola destructor (Say) (Diptera: Cecidomyiidae), has been identified as (10E)-tridecen-2-yl acetate. A flexible synthetic route was developed which allowed access to the chiral and racemic forms of the pheromone, and to the 10Z stereoisomer of the pheromone. The natural compound was determined to have the 2S configuration by hydrolysis of the acetate function, derivatization of the resulting alcohol with (2S)-2-acetoxypropionyl chloride, and capillary gas Chromatographic comparison of the derivative with the corresponding derivatives prepared from the synthetic enantiomers. Trace amounts of the 10Z isomer of the pheromone have also been detected in extracts of female Hessian fly ovipositors, along with (10E)-tridecen-2-ol and 2-tridecanyl acetate. Due to the small quantities of these compounds available from ovipositor extracts, the chirality of the trace components has not yet been determined.     

Variation in host fruit volatiles attractive to apple maggot fly,Rhagoletis pomonella

We conducted a comparative study of volatiles produced by wholeCrataegus hawthorn fruit and four cultivars of apple (Royal Red Delicious, Red Astrachan, McIntosh, and Wealthy) and determined quantitative and qualitative changes of volatiles associated with fruit ripening. Within the approximate range of the GLC fraction known to elicit behavioral activity in the apple maggot fly,Rhagoletis pomonella (Walsh) (Diptera: Tephritidae), 52 esters were identified.     

House fly oviposition inhibition by larvae ofHermetia illucens,the black soldier fly

Wild populations of house flies were inhibited from ovipositing into poultry manure containing larvae of the black soldier fly,Hermetia illucens (L.). A laboratory strain of house fly responded differently, readily ovipositing into manure with lower densities of soldier fly larvae, but avoiding the higher densities tested. The amount of timeH. illucens larvae occupy the manure prior to an oviposition test influences ovipositional responses of house flies. Manure conditioned byH. illucens larvae for 4–5 days did not significantly inhibit house fly oviposition. We suggest that some type of interspecific chemical communication (allomone) is present.Diptera: Stratiomyidae.Portion of an MS thesis by S.W.B.Research partially supported by State and Hatch funds.     

Onion fly trap catch as affected by release rates ofn-dipropyl disulfide from polyethylene enclosures

n-Dipropyl disulfide loadings of at least 1 l and 10 l in polyethylene enclosures were required to effect significant trap catches of onion fly,Hylemya antiqua (Meigen), females and males, respectively. Corresponding release rates for this threshold for trap catch were ca. 100 g/hr. Catches increased with loadings up to 100 l/capsule but then plateaued. As determined gravimetrically, the release rate from enclosures containing a reservoir of chemical remained constant under isothermal conditions but increased exponentially as a function of temperature.Diptera: AnthomyiidaePaper No. 9422 of the Michigan State University Agricultural Experiment Station. Received for publication April 29, 1980.     

Oviposition in Delia platura (Diptera, Anthomyiidae): The Role of Volatile and Contact Cues of Bean

The choice of a suitable oviposition site by female insects is essential for survival of their progeny. Both olfactory and contact cues of the oviposition site may mediate this choice. The polyphagous Delia platura (Diptera: Anthomyiidae), a severe agricultural pest of numerous crops, lays eggs in the soil close to germinating seeds. Maggots feed upon the cotyledons. Only little is known about the cues guiding oviposition behavior. In this study, the effects of both olfactory and contact cues of beans (Phaseolus vulgaris) on oviposition of D. platura females were tested. Egg deposition on germinated beans was preferred to egg deposition on ungerminated beans or on beans in different postgerminating developmental stages. Olfactory cues of germinating beans alone stimulated female flies to lay eggs. Additional contact cues of germinating beans seemed to enhance the response, but the difference was not significant. Surface extracts of germinating beans sprayed on surrogate beans showed that both polar and nonpolar substances stimulated oviposition of D. platura flies. Gas chromatography-electroantennographic detection recordings of head space samples of germinating beans showed positive response of females to different compounds. We conclude that olfaction plays a major role when D. platura females are searching for oviposition sites. Volatile compounds released from germinating beans such as 4-hydroxy-4-methyl-2-pentanone, 1-hepten-3-one, 1-octen-3-ol, and 3-octanone should be considered as key compounds that mediate oviposition behavior. The use of different sensory modalities by closely related species of Delia is discussed.     

Olfactory Responses of the Predatory Mites (N eoseiulus cucumeris) and Insects (O rius strigicollis ) to Two Different Plant Species Infested with Onion Thrips (T hrips tabaci)

Responses of Neoseiulus cucumeris (a predatory mite) and the predatory insect Orius strigicollis to volatiles associated with two different plant species infested with onion thrips, Thrips tabaci, were examined in a Y-tube olfactometer. Both predators species showed a significant preference for volatiles from infested cucumber leaves without T. tabaci over clean air. However, they were not attracted to volatiles from uninfested cucumber leaves, artificially damaged cucumber leaves, or volatiles from T. tabaci plus their visible products collected from cucumber leaves. These results suggest that both predator species are capable of exploiting herbivore-induced volatiles from T. tabaci-infested cucumber leaves as a foraging cue. Neither predator was attracted to volatiles from uninfested spring onion leaves, infested spring onion leaves without T. tabaci, or volatiles from T. tabaci plus their visible products collected from spring onion leaves. Interestingly, they avoided volatiles from artificially damaged spring onion leaves. A possible explanation for the non-significant olfactory responses of the predator species to spring onion plants with infestation damage of T. tabaci is discussed.     

Tolerance of <Emphasis Type="Italic">Drosophila</Emphasis> Flies to Ibotenic Acid Poisons in Mushrooms

The mushroom genus Amanita has a spectrum of chemical compounds affecting survival and performance of animals. Ibotenic acid is one of such compounds found in some Amanita mushrooms. We studied the effects of ibotenic acid and its derivative, muscimol, on egg-to-pupa survival, pupation time, and pupal size in five Drosophila species (Diptera: Drosophilidae), Drosophila bizonata, Drosophila angularis, Drosophila brachynephros, Drosophila immigrans, and Drosophila melanogaster. The first three species are mycophagous and use a wide range of mushrooms for breeding, whereas D. immigrans and D. melanogaster are frugivorous. We reared fly larvae on artificial medium with 500, 250, 125, and 62.5 μg/ml of ibotenic acid and/or musimol. The three mycophagous species were not susceptible to ibotenic acid, whereas the two frugivorous species were affected. In experiments with D. melanogaster, muscimol was less toxic than ibotenic acid.     

Factors Accounting for the Variability in the Behavioral Response of the Onion Fly (Delia antiqua) to n-Dipropyl Disulfide

The onion fly Delia antiqua is a specialist herbivore attacking only onions and closely related Allium species. n-Dipropyl disulfide (Pr₂S₂) has long been known to be attractive to onion flies in the laboratory and in the field. However, the insect's response is highly variable. Using behavioral bioassays we found that Pr₂S₂ was highly attractive to gravid, mated female onion flies, but did not stimulate oviposition. The response of female onion flies was concentration dependent. The physiological state of the flies (i.e., age, mating status, egg load/oviposition experience) also affected their responsiveness. The response of both sexes of onion flies varied with age, but females were always more strongly attracted than males. Responsiveness of females increased during the first 10 days after emergence. It stayed at a high level until 21 days after which the experiment was terminated. The responsiveness of males reached a maximum at 6–7 days after which it declined. Mated, gravid females responded more strongly to Pr₂S₂ than unmated, gravid females. Females deprived of the opportunity to oviposit were more attracted compared to females that had oviposited on cut onions prior to the experiment. Electroantennograms (EAG) of females revealed a higher response to stimulation compared to males. The EAG-response of females was not affected by mating status.     

A mating stimulant pheromone of the horn fly,Haematobia Irritans (L.): Demonstration of biological activity in separated cuticular components

Preliminary bioassays with the horn fly,Haematobia irritans (L.), suggested that a mating stimulant pheromone was involved in horn fly courtship behavior. Virgin males readily courted live or dead females but rarely courted live males, dead males, or females thoroughly washed with hexane. The bioassay used was the response of virgin males to treated male horn flies. Results indicated that female cuticular hydrocarbons induced male courtship behavior. Specifically, the female paraffin and monoolefin fractions were biologically active when bioassayed alone or in combination. Three synthetic monoolefins previously shown to be the major components in the female monoolefin fraction were active in bioassays. The compoundsZ-5-tricosene,Z-9-pentacosene, andZ-9-heptacosene were each active, but greater male courtship behavior was observed when these three compounds were bioassayed in combination.Diptera: Muscidae.A portion of a dissertation by the first author to the graduate school of the University of Florida in partial fulfillment of the requirements for the PhD degree.Florida Agricultural Experiment Station Journal Series No. 2078.Mention of a proprietary or commercial product does not constitute an endorsement by either the University of Florida or the U.S. Department of Agriculture.     

Pungent spices,ground red pepper,and synthetic capsaicin as onion fly ovipositional deterrents

In laboratory choice experiments, the spices dill, paprika, black pepper, chili powder, ginger, and red pepper deterredDelia antiqua oviposition by 88–100%. Dose-response choice tests demonstrated that 1 mg of ground cayenne pepper (GCP) placed within 1 cm of artificial onion foliage reduced oviposition by 78%. A synthetic analog of capsaicin, the principal flavor ingredient of red peppers, deterred oviposition by 95% when present at 320 ppm in the top centimeter of sand (the ovipositional substrate). However, in no-choice conditions 10 mg GCP was not an effective deterrent. Sevana Bird Repellent and Agrigard Insect Repellent both use red pepper as a principal ingredient; at recommended field rates, neither of these materials was an effective ovipositional deterrent either in laboratory or field. Capsaicin-based materials do not appear to be candidates for onion maggot control via behavioral modification.Paper No. 12514 of the Michigan Agricultural Experiment Station.