Earthworm mucus stimulates oviposition in a predatory fly (Diptera: Anthomyiidae)

Coenosia tigrina larvae feed on earthworms. We hypothesized that earthworm mucus contains a kairomone that stimulates oviposition behavior in adultC. tigrina females, thus minimizing the search area in the soil required for newly eclosed larvae to find earthworms. In bioassays, adult females responded with extension of the ovipositor 25–43% of the time to earthworm-mucus-soaked filter paper disks compared to 6–7% in response to water-soaked disks. Ovipositor extension on mucus-soaked disks was followed by egg-laying 29% of the time and 0% of the time on water-soaked disks. Egg-laying byC. tigrina followed a diurnal periodicity, with most eggs laid in the latter half of the photophase even in the absence of earthworm mucus. More eggs were deposited from 1600 to 1800 hr by females given access to earthworm mucus during that period than were deposited by females not given access. There was no difference in the number of eggs deposited from 0600 to 0800 hr, by females given access to earthworm mucus or not. This is a time of day when few eggs are normally laid. This paper is the first report of an earthworm-produced kairomone in an insect-earthworm interaction. The kairomone may have potential for enhancing biological control of the onion maggot,Delia antiqua, which is a prey of adultC. tigrina.     

Influence of trichome exudates from species ofLycopersicon on oviposition behavior ofHeliothis zea (Boddie)

Cage experiments revealed that accessions of the wild tomato speciesLycopersicon hirsutum were preferred sites for oviposition byHeliothis zea. Hexane extracts from the leaves ofL. hirsutum were also preferred sites of oviposition in choice experiments among extracts from severalLycopersicon species. Extracts ofL. hirsutum were still biologically active several days after application, indicating that the phytochemical(s) involved are relatively stable and of low volatility. Gas Chromatographic analysis of leaf hexane extracts from 12 different accessions of theL. hirsutum complex and three tomato cultivars revealed substantial qualitative and quantitative variation in the chemical composition of these extracts. Comparison of these results with extract oviposition studies implicate a group of structurally related compounds as the active agents. Mass spectroscopy has tentatively identified these compounds as sesquiterpenes with the chemical formula C₁₅H₂₂O₂. These compounds are apparently synthesized and secreted from glandular trichomes on the leaf surface. These phytochemicals did not stimulate ovipositional behavior in females of the cabbage looper,Trichoplusia ni. The existence of genetic variation for the presence and amount of kairomones that serve as cues for insect orientation and oviposition could be utilized in a breeding program to develop tomato cultivars with genetically modified allelochemic profiles that would disrupt the sequential behavioral processes of insect host-plant selection.     

Field evaluation of synthetic compounds mediating oviposition inCulex mosquitoes (Diptera: Culicidae)

3-Methylindole (skatole), a compound shown to be an oviposition attractant/stimulant forCulex quinquefasciatus in laboratory tests, was evaluated against natural populations of mosquitoes in the field. In experiments using paired black plastic tubs that contained water treated with an attractant solution containing a mixture of 3-methylindole, 4-methylphenol, 4-ethylphenol, phenol, and indole or that contained only tap water, the attractantbaited traps received significantly moreCx. quinquefasciatus egg rafts than did the untreated tap water. Gravid female traps that were baited with attractant solution collected significantly moreCx. quinquefasciatus females than did traps containing only tap water. There was no significant difference in number ofCx. quinquefasciatus collected in the traps baited with the attractant solution compared to the traps that contained water with 3-methylindole alone, indicating that 3-methylindole was solely responsible for the attraction. In replicated experiments conducted in experimental ponds, ponds that were treated with 3-methylindole received significantly moreCx. quinquefasciatus, Cx. tarsalis, andCx. stigmatosoma egg rafts than did untreated ponds. Experimental ponds treated with 3-methylindole at two levels (0.12 and 0.6 mg/liter) were equally attractive to ovipositingCx. quinquefasciatus. This is the first record of 3-methylindole showing attractancy/stimulation to ovipositingCx. stigmatosoma andCx. tarsalis under field or laboratory conditions.     

Volatile compounds in the larval frass ofDendroctonus valens andDendroctonus micans (Coleoptera: Scolytidae) in relation to oviposition by the predator,Rhizophagus grandis (Coleoptera: Rhizophagidae)

During a laboratory study evaluatingRhizophagus grandis (a specific native predator of the Eurasian bark beetle,Dendroctonus micans), as a potential biocontrol agent against the North American bark beetle,Dendroctonus valens, it was found that feeding larvae and laboratory-produced frass of the potential prey elicited very high oviposition responses in the predator. Comparative chemical analysis of this laboratory-produced larval frass revealed that one major volatile compound, (-)-fenchone, is associated with the larvae of bothDendroctonus species.D. micans also generated pinocamphone while oxygenated monoterpenes in the frass ofD. valens were camphor,cis-4-thujanol, fenchol, terpinen-4-ol, myrtenal, pinocarvone, borneol, verbenone, piperitone, campholenaldehyde,trans-myrtanol,cis-myrtanol,p-cymen-8-ol and 5-oxo-camphor. This range of prey-produced compounds with a possible biological effect onR. grandis was narrowed down subsequent to comparative analysis of field-collected larval frass. (-)-Fenchone, pinocamphone, camphor, terpinen-4-ol, borneol, fenchol, and verbenone were found to be common to both prey species. A mixture of these seven components was tested in a bioassay, where it elicited as much oviposition as did larval frass ofD. micans. The oviposition stimulants forR. grandis are thus clearly among the mixture's constituents.     

Kairomones and their use for management of entomophagous insects. IV. Effect of kairomones on productivity and longevity ofTrichogmmma pretiosum riley (Hymenoptera: Trichogrammatidae)

Kairomones in the scales ofHeliothis zea (Boddie) increased the percent parasitization, the number of progeny produced, and the longevity of femaleTrichogramma pretiosum Riley.In cooperation with the University of Georgia College of Agriculture Experiment Station, Coastal Plain Station, Tifton, Georgia 31794.Mention of a commercial or proprietary product in this paper does not constitute endorsement by the USDA.     

Deterrence of repeated oviposition by fruit-marking pheromone inCeratitis capitata (Diptera: Tephritidae)

During ovipositor dragging on the fruit surface following egg laying in hawthorne fruit,Ceratitis capitata (Wiedemann) females deposit an unidentified pheromone that deters repeated oviposition attempts in that fruit. The pheromone proved water soluble and, when collected and sprayed in aqueous solution onto uninfested fruits in laboratory cages, effectively deterred boring attempts byC. capitata females of wild origin for at least 6 days (termination of test). A laboratory population ofC. capitata cultured on artificial media for more than 200 generations deposited pheromone that proved equally as deterrent to wild fly oviposition as pheromone from wild flies. However, lab fly oviposition was not effectively deterred by the presence of pheromone. The ecological significance of the pheromone is discussed.     

Female-produced oviposition deterrents of the cigarette beetle,Lasioderma serricorne (F.) (Coleoptera: Anobiidae)

Oviposition deterrents of the cigarette beetle,Lasioderma serricorne, were isolated from its adult body extract and found to be identical to (2S,3R,1'S)-2,3-dihydro-3,5-dimethyl-2-ethyl-6-(l-methyl-2-oxobutyl)-4H-pyran-4-one (-serricorone) and its lR-epimer (-serricorone) by spectroscopic evidence. Serricorone was previously found as one of the minor sex pheromone components of the same insect, and hence indicating bi-functional nature. The presence of two isomers in the body was proved by careful treatment. Each of them exhibited the same level of oviposition deterring activity, which was less potent than the crude body extract at an increased concentration.     

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.     

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.     

Response ofMeteorus leviventris, (Hymenoptera: Braconidae) to mustard oils in field trapping experiments

Trapping experiments were carried out near Saskatoon, Canada, from May through August 1990 to assess the response of the braconid wasp,Meteorus leviventris, to four selected mustard oils or isothiocyanates (IC) at a release rate of 4 mg/day, and for allyl IC only, at 40 mg/day. Only allyl IC at 4 mg/day was significantly attractive when trap captures were compared to the captures in the control traps. The others (n-propyl IC, 2-phenylethyl IC., and ethyl IC) were not attractive, nor was allyl IC at the higher dose, although trap captures with the latter bait were the second highest.     

Mating stimulant pheromone and cuticular lipid constituents ofFannia femoralis (Stein) (Diptera: Muscidae)

The cuticular lipids of male and femaleFannia femoralis were similar for recently emerged insects but soon began to develop chromatographic patterns characteristic of each sex. Mature females contained more C₃₁ and C₃₃ monoolefin in the cuticular lipid than males. Also, the double bonds in the monoolefins of the female lipid were situated predominantly at the eleventh and thirteenth carbons, while most of those from the males were centrally located in the molecule or at the ninth carbon.The female C₃₁ monoolefin stimulated copulation by the males, but more mating activity occurred when the saturated hydrocarbons present in the female cuticular lipids were added. The synthetic monoolefin most active as a mating stimulant pheromone was (Z)-11-hentriacontene, but the addition of female alkanes or of syntheticn-alkanes to (Z)-11-hentriacontene increased the activity of the synthetic pheromone.A portion of a dissertation intended for submission by the first author to the Graduate School of the University of Maryland in partial fulfillment of the requirements for the Ph.D. degree.Mention of a proprietary or commercial product in this paper does not constitute an endorsement of this product by the U.S. Department of Agriculture or the University of Maryland.     

Evaluation of organic infusions and synthetic compounds mediating oviposition inAedes albopictus andAedes aegypti (Diptera: Culicidae)

Oviposition responses of gravidAedes albopictus andAe. aegypti were evaluated to natural organic infusions (hay infusion, larval rearing water, and field-collected larval water) as well as compounds isolated from hay infusion (3-methylindole, 4-methylphenol, 4-ethylphenol, indole, and phenol) known to elicit oviposition inCulex mosquitoes. In laboratory bioassays, significant oviposition responses were obtained fromAe. albopictus, but not fromAe. aegypti, to dilutions of hay infusion and field water. Oviposition responses of both species were moderate to the synthetic compounds tested in the laboratory (0.01–100 µg/liter). Only 3-methylindole (0.1 µg/liter) and 4-ethylphenol (1.0 µg/liter) elicited significantly more oviposition byAe. albopictus than did well water. Of the synthetic compounds tested withAe. aegypti, only phenol (1.0 µg/liter) and 4-ethylphenol (0.1 µg/liter) elicited significantly more oviposition than did well water. Significant repellency or oviposition deterrence for both species occurred in response to at least one high concentration of most of the compounds tested. In field cage evaluations, oviposition responses byAe. albopictus were strongest to larval water and field water, moderate to hay infusion and 3-methylindole (100 µg/liter), and low to well water. A mixture of five synthetic compounds mimicking hay infusion was no more effective than 3-methylindole alone. ForAe. aegypti, oviposition responses were greatest to larval water and least to 3-methylindole. In an olfactometer, gravid females of both species oriented more to field water than to well water and onlyAe. albopictus oriented more to larval water or hay infusion than well water. In general, gravidAe. albopictus responded more strongly to oviposition stimuli than didAe. aegypti.     

Role of volatile inforchemicals emitted by feces of larvae in host-searching behavior of parasitoidCotesia rubecula (Hymenoptera: Braconidae): A behavioral and chemical study

The role of volatile infochemicals emitted by feces of larvae in the host-searching behavior of the parasitoidCotesia rubecula was evaluated during single- and dual-choice tests inside a wind tunnel. The following treatments were tested: feces produced by second and fourth instars ofPieris rapae (preferred host), second instars ofP. brassicae (inferior host), second instars ofP. napi (nonhost), and wet feces of second instars ofP. rapae. During a single-choice situation females ofC. rubecula oriented to all types of feces tested. When a preference was to be made,C. rubecula preferred feces of second instars ofP. rapae over that of fourth, feces ofP. rapae over that ofP. brassicae, feces ofP. napi over that ofP. brassicae, and wet over normal host feces. No preference was exhibited between feces of second instars ofP. napi and that of second instars ofP. rapae. The relative importance of infochemicals from host feces versus plant damage caused by host larvae to the searching behavior ofC. rubecula was also evaluated. Plant damage was more important to the searching females than host feces when feces were present in specific concentrations in relation to damage. The volatiles released by normal and wet feces of second instars ofP. rapae, wet feces of fourth instars ofP. rapae, and normal and wet feces ofP. brassicae were collected and identified. Overall, 85 chemical compounds were recorded belonging to the following chemical groups: alcohols, ketones, aldehydes, esters, isothiocyanates, sulfides, nitriles, furanoids, terpenoids and pyridines. The blend of chemicals emitted by feces of different instars ofP. rapae and different species ofPieris exhibited an instar and species specificity in both quantity and quality. Wetting of normal feces increased the amount of volatile chemicals released, and it was also responsible for the appearance of new compounds. The role of feces of larvae in the host-seeking behavior ofC. rubecula is discussed.     

Foliar chemicals of wheat and related grasses influencing oviposition by Hessian fly,Mayetiola destructor (Say) (Diptera: Cecidomyiidae)

More than twice the number of mated female Hessian flies,Mayetiola destructor (Say) entered a zone within 1 cm of a paper strip treated with one plant equivalent (PE) of a chloroform extract of wheat foliar waxes compared to a strip treated with solvent only; females also stayed six times longer and laid 10 times more eggs on the strip treated with the wheat extract. Column chromatographic fractionation of the wheat extract and application of these fractions onto filter paper strips showed four fractions elicited significant numbers of eggs to be laid. Single, binary, and tertiary combinations of three of these fractions (two of the four fractions apparently contained similar compounds) were tested. The greatest numbers of eggs were laid on strips treated with the tertiary combination or the binary combination conaining the two most active fractions (3 and 6); three times the number of eggs were laid on strips treated with this binary combination than the sum of eggs laid on strips treated with these two fractions separately. A comparison of grasses and their extracts showed female Hessian flies laid greater numbers of eggs on wheat or rye than on barley or oat. Fractionated barley and oat extracts were tested for activity as for wheat, and a similar pattern was observed, i.e., the greatest numbers of eggs were laid on fractions 3 and 6. Dose-response tests, using these two fractions of wheat, barley, or oat showed the same threshold of activity for fraction 3 for all three extracts, i.e., 2 PE. In contrast, fraction 6 of wheat was active at the lowest dosage tested, 0.25 PE, while the same fraction of either barley or oat was not active until tested at a dosage of 2 PE. It appears that (at least) two chemicals in the foliar waxes of these grasses influence ovipositional behavior of female Hessian flies. Furthermore, given the similar foliar chemistry of these grasses and the strong synergistic interaction between fractions 3 and 6 shown for wheat extract, it is likely that the ovipositional preferences exhibited by female Hessian flies towards these grasses may be explained by quantitative differences in the amount(s) of the active chemical(s) in their respective fraction 6 (most polar fraction tested).     

Synergism between chemical attractants and visual cues influencing oviposition of the mosquito,Culex quinquefasciatus (Diptera: Culicidae)

Physical factors, such as the color of the oviposition substrate, have seldom been compared with chemical cues in their ability to elicit oviposition behavior in mosquitoes. The role of dyed oviposition waters in attracting ovipositingCulex quinquefasciatus was examined in laboratory experiments. Oviposition waters dyed with ink were found to be significantly attractive to ovipositingCx. quinquefasciatus when compared to distilled water controls. Experiments demonstrated that the mosquitoes were responding to the increased optical density of the dyed oviposition water rather than volatile components of the dye. Ink was also considered in combination with chemical oviposition cues. No comparative data exist on the effect of physical and chemical factors presented together on the oviposition behavior ofCx. quinquefasciatus. Waters dyed with ink acted synergistically with a five-component chemical attractant mixture (3-methylindole, indole, 4-methylphenol, 4-ethylphenol, and phenol) in inducing oviposition in a 2×2 factorial experiment.     

Intensification and prolongation of host searching inLeptopilina heterotoma (Thomson) (Hymenoptera: Eucoilidae) through a kairomone produced byDrosophila melanogaster

A chemical cue (kairomone) of the host, larvae ofDrosophila, was found to influence patch-time allocation of the parasiteLeptopilina heterotoma. This kairomone is soluble in water and chloroform. The kairomone was purified using thin-layer chromatography. The concentration of the kairomone increases with an increasing number of hosts. The parasites may use presence and concentration of the kairomone as cues to determine patch-time allocation.     

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.     

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.     

Wind tunnel studies of sex pheromone-mediated behavior of the Hessian fly (Diptera: Cecidomyiidae)

In a wind-tunnel, male Hessian flies flying toward a source of the female-produced sex pheromone exhibited flight maneuvers very similar to those described for male moths. Upwind flight, consisting of zigzagging and straight flight upwind, was initiated within seconds after flies were placed in the odor plume. This upwind flight was sometimes interrupted by casting, which consisted of wide excursions in the horizontal plane ranging 10–35 cm across the central zone of the tunnel. Comparison of the flight maneuvers of males exposed to ten female equivalents of a hexane extract of female ovipositors and males exposed to 20 ng of (2S)-(E)10-tridecen-2-yl acetate (SE10-13:OAc), which has been identified as a component of the Hessian fly sex pheromone, indicated that the sex pheromone probably contains additional components. However, SE10-13: OAc elicited upwind flight and source location by a significant number of males, even at dosages as low as 2 ng on filter paper. At the highest dosage of SE10-13:OAc tested (200 ng on filter paper), there was a significant decrease in net flight velocity and a slight, but not significant, reduction in the number of males contacting the odor source. The addition of increasing amounts of the R enantiomer to the S enantiomer resulted in increased inhibition of upwind flight and source contact by males.     

Suppression of oviposition inOryzaephilus surinamensis (L.) (Coleoptera: Cucujidae) following prolonged retention in high-density cultures or short-term exposure to larval volatiles

After 20 days in a high-density culture containing many larvae, female sawtoothed grain beetles,Oryzaephilus surinamensis (L.), laid half as many eggs in a 24-hr oviposition bioassay as females held for six days in the same culture, or for six or 20 days in a low-density culture. Oviposition by females held for six days in a high-density culture was reduced to a similar extent when they were exposed in the oviposition bioassay to an oat flake treated with an extract of Porapak Q-captured larval volatiles (equivalent to 5000 larval hours). A retained suppression of oviposition rate after prolonged exposure to larvae or an induced reduction caused by short-term exposure to larval volatiles both could be of adaptive advantage in reducing the risk of oviposition in an already densely populated habitat.Research supported by the Natural Sciences and Engineering Research Council of Canada, Strategic Grant G0958 and Operating Grants A3881 and A3785.