Kairomones for the egg parasiteTrichogramma evanescens Westwood

In observation-cage experiments some new contact kairomones for the egg parasiteTrichogramma evanescens Westwood are demonstrated.T. evanescens females search significantly longer on cabbage leaves treated with the wing scales of two hosts,Pieris brassicae L. andP. rapae L. Further, egg washes ofP. brassicae containing an oviposition deterrent pheromone for the butterflies, were found to have a contact-kairomonal effect on the parasite.T. evanescens females search significantly longer on cabbage leaves sprayed with a methanol or water wash ofP. brassicae eggs than on leaves treated with the solvent only.Hymenoptera: Trichogrammatidae.Lepidoptera: Pieridae.     

Evidence for a Host-Marking Pheromone in White Spruce Cone Fly, Strobilomyia neanthracina

Cone flies (Strobilomyia spp.) lay eggs on coniferous cones, and larvae must complete development within the cone on which the eggs are laid. Previous field surveys showed that egg distributions of several species are uniform, suggesting that females avoid ovipositing on cones with conspecific eggs or larvae. In both the field and laboratory, S. neanthracina females walked around cones following oviposition, touching their mouthparts to the cone as they walked. In laboratory bioassays, where females were presented with a cone on which they or another female had oviposited and touched with mouthparts, or one without an egg, females laid preferentially on cones without eggs. However, females laid randomly when presented with a cone on which a female had oviposited but been prevented from touching with her mouthparts following oviposition or another cone without an egg. This indicates that females deposit a host-marking pheromone with their mouthparts following oviposition and that this deters further oviposition on marked hosts. Laboratory and field bioassays indicated that the host-marking pheromone is located in the head and thorax of female flies.     

Plant response to eggs vs. Host marking pheromone as factors inhibiting oviposition byPieris brassicae

Pieris brassicae L. butterflies secrete miriamides onto their eggs. These avenanthramide alkaloids are strong oviposition deterrents when sprayed onto a cabbage leaf. However, these compounds could not be detected in cabbage leaves from which egg batches had been removed two days after deposition and that still showed oviposition deterrency. It was concluded that the miriamides were not directly responsible for the avoidance by females of occupied leaves while searching for an oviposition site. Evidence was obtained that cabbage leaves themselves produce oviposition deterrents in response to egg batches. Fractions containing potent oviposition deterrents could be isolated from surface extracts of leaves from which previously laid egg batches had been removed. The term host marking pheromone that was used previously is not applicable in this case.     

Lonicera Implexa Leaves Bearing Naturally Laid Eggs of the Specialist Herbivore Euphydryas Aurinia have Dramatically Greater Concentrations of Iridoid Glycosides than other Leaves

We tested in the field the hypothesis that the specialist butterfly Euphydryas aurinia (Lepidoptera: Nymphalidae, Melitaeinae) lays eggs on leaves of Lonicera implexa (Caprifoliaceae) plants with greater iridoid concentrations. We conducted our investigations in a Mediterranean site by analyzing leaves with and without naturally laid egg clusters. There were no significant differences in iridoid glycoside concentrations between leaves from plants that did not receive eggs and the unused leaves from plants receiving eggs, a fact that would seem to indicate that E. aurinia butterflies do not choose plants for oviposition by their iridoid content. However, the leaves of L. implexa that bore egg clusters had dramatically greater (over 15-fold) concentrations of iridoid glycosides than the directly opposite leaves on the same plant. These huge foliar concentrations of iridoids (15% leaf dry weight) may provide specialist herbivores with compounds that they either sequester for their own defense or use as a means of avoiding competition for food from generalist herbivores. Nevertheless, it may still be possible that these high concentrations are detrimental to the herbivore, even if the herbivore is a specialist feeder on the plant.     

Induction of Plant Synomones by Oviposition of a Phytophagous Insect

Earlier investigations of host habitat location in the egg parasitoid Oomyzus gallerucae have shown that oviposition of the elm leaf beetle (Xanthogaleruca luteola) induces the field elm (Ulmus minor) to emit volatiles that attract the egg parasitoid. In this study we investigated the mechanism of this induction by testing the effects of differently treated elm leaves on O. gallerucae in a four-arm olfactometer. First we investigated which sequence of the herbivore oviposition behavior is necessary for the synomone induction. The following major sequences were observed: (1) Prior oviposition, the gravid female gnawed shallow grooves into the leaf surface. (2) After gnawing upon the leaf surface, the female attached about 20–30 eggs with oviduct secretion in the grooves. We experimentally mimicked the shallow grooves on the leaf surface by scratching the leaf surface with a scalpel (= scratched leaves). Volatiles from such scratched leaves did not attract the egg parasitoid. However, as soon as eggs with oviduct secretion, or only oviduct secretion, was applied to these scratched leaves, they emitted attractive volatiles. Application of oviduct secretion and eggs on undamaged leaves did not elicit release of attractive synomones. Thus, an elicitor is located in the oviduct secretion, but becomes active only when the leaf surface is damaged. Jasmonic acid is known as a mediator of plant responses induced by feeding of herbivorous arthropods, and we demonstrate that it mediates production of elm synomones that attract O. gallerucae. The plant's reaction to oviposition was systemic, and leaves without eggs near leaves with eggs emitted attractants.     

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.     

Influence of Host-Plant Surface Chemicals on the Oviposition of the Cereal Stemborer Busseola Fusca

The chemical composition of plant surfaces plays a role in selection of host plants by herbivorous insects. Once the insect reaches the plant, these cues determine host acceptance. Laboratory studies have shown that the stem borer Busseola fusca (Lepidoptera: Noctuidae), an important pest of sorghum and maize in sub-Saharan Africa, is able to differentiate between host and non-host plant species. However, no information is available on the cues used by this insect to seek and accept the host plant. Thus, the role of surface phytochemical stimuli on host selection and oviposition by B. fusca was studied in the laboratory using two host plants, sorghum, Sorghum bicolor, and maize, Zea mays, and one non-host plant, Napier grass, Pennisetum purpureum. The numbers of eggs and egg masses deposited on the three plant species were compared first under no-choice and choice conditions. In both cases, more eggs and egg masses were laid on maize and sorghum than on the non-host. Artificial surrogate stems treated with a water or chloroform surface extract of each plant were then compared with surrogate stems treated with, respectively, water or chloroform as controls, under similar conditions. Surrogate stems treated with plant water extracts did not show an increase in oviposition when compared to controls, indicating that the major compounds in these extracts, i.e., simple sugars and free amino acids, are not significantly responsible for the oviposition preference. By contrast, a chloroform extract of sorghum enhanced oviposition on the surrogate stems compared to the control, while those of maize and Napier grass showed no significant effects. Analysis of the chloroform extract of sorghum showed higher amounts of α-amyrin, ß-amyrin, and n-nonacosane compared to those of maize and Napier grass. A blend of the three chemicals significantly increased oviposition compared to the chloroform-treated control, indicating that these compounds are part of the surface chemical signature of the plant responsible for host recognition and oviposition by B. fusca.     

Experience Induces a Phytophagous Insect to Lay Eggs on a Nonhost Plant

Experience of nonhost plants by phytophagous insects may alter their foraging and oviposition responses to these plants. Using the diamondback moth (DBM) Plutella xylostella (L.), its host-plant Chinese cabbage, and a nonhost-plant Pisum sativum (pea) as a model system, we examined whether experience of the nonhost plant by adults can induce oviposition on the nonhost plant. Naive DBM females did not accept pea for oviposition in either no-choice or choice conditions, whereas females with prior experience of pea laid up to 20% of their eggs on this plant. Naive females reduced their oviposition, but experienced females did not refrain from laying eggs in a nonhost-plant environment. Such habituation to nonhost plants could lead to host range expansion in phytophagous insects and increase mortality of pest insects in diversified crop systems.     

Aggregated oviposition inDelia antiqua (Meigen): A case for mediation by semiochemicals

Experiments conducted in the laboratory tested the hypotheses that aggregated oviposition by onion maggot flies,Delia antiqua (Meigen), is caused by stimuli associated with ovipositing females, newly laid eggs, or both. Using a paired oviposition station bioassay that eliminated visual stimuli associated with the treatment under study, 67% of the eggs laid by caged females were in response to the odor of females already ovipositing on an onion slice, as opposed to 33% of the eggs laid in response to an onion slice alone. When newly laid eggs were transferred to onion slices and held for either 24 or 48 hr before being bioassayed against similarly aged untreated onions, 74% and 97% of the eggs were laid at the egg-treated onion stations, respectively. Similar results were achieved when an aqueous wash of newly laid eggs was applied to the onion slice. When the egg wash was processed through a bacterial filter or when eggs were present but not in contact with onions, all response was eliminated. These results implicate microorganisms transmitted on the egg surface in creating an attraction for ovipositing females. Heptane extracts of ovipositor tips from mated, ovipositing females induced 72% of the test females to oviposit near points at which extracts were applied to the oviposition station floor. A behavioral sequence for an optimal host-selection strategy is hypothesized, whereby host-seeking female onion flies respond to host-derived alkyl sulfides at long range and metabolic by-products of microbially infested hosts and visual cues at short range (ca. l m), with final selection of oviposition sites potentially reinforced by contact with an aggregation pheromone released or left on the substrate by ovipositing females.     

Isolation and identification of oviposition deterrents to cabbage butterfly,Pieris rapae,fromErysimum cheiranthoides

Avoidance of some crucifer species by the crucifer specialist,Pieris rapae, has been attributed to the presence of oviposition deterrents in these plants. Studies on one such unacceptable plant,Erysimum cheiranthoides, have resulted in the isolation ofn-butanol-soluble deterrents from the alcoholic extract of foliage. The active fraction contained three cardiac glycosides, which were isolated by reversed-phase HPLC and by open column chromatography on silica gel. Chemical and spectral evidence (UV, [¹H]NMR, and FAB-MS) led to the characterization of these compounds as erysimoside (1), erychroside (2), and erycordin (3). Erysimoside and erychroside were strongly deterrent toPieris rapae, but erycordin was inactive. Both active compounds have the same aglycone, strophanthidin (5) and the inner sugar in both cases is a 2,6-dideoxy hexose to which the outer sugar is attached at position C-4. These structural features, which are absent in the inactive compound (3), may represent specific requirements for oviposition deterrent activity.     

Hydroxybenzoic Acid Derivatives in a Nonhost Rutaceous Plant, Orixa japonica, Deter Both Oviposition and Larval Feeding in a Rutaceae-Feeding Swallowtail Butterfly, Papilio xuthus L.

A Rutaceae-feeding swallowtail butterfly. Papilio xuthus L., feeds on various rutaceous plants but always rejects Orixa japonica Thunb. (Rutaceae). Females were strongly deterred from laying eggs by a methanolic extract of O. japonica leaves. Larvae also rejected a diet leaf medium impregnated with O. japonica leaf extracts. Several components in the water-soluble fraction of the leaf extract were found to deter both oviposition and feeding responses. Two major deterrent compounds were characterized as 5-[[2-O-(beta-D-apiofuranosyl)-beta-D-glucopyranosyl]oxy]-2-hydroxybenzoic acid and adisyringoyl aldaric acid. These compounds induced potent deterrence of both oviposition and larval feeding by P. xuthus, which suggests a congruent chemosensory mechanism of allomonal chemicals acting on both female tarsal chemoreceptors and larval maxillary taste receptors.     

Volatile Plant Infochemicals Mediate Plant Preference of Trichogramma chilonis

In India, eggs of the polyphagous noctuid moth Helicoverpa armigera on sorghum are parasitized to high levels by Trichogramma spp., but only rarely are parasitized eggs found on pigeonpea. This study was conducted to test whether volatile plant infochemicals contribute to the different parasitism levels observed on these two crops. In a four-armed airflow olfactometer, volatiles emitted by both sorghum and pigeonpea plants elicited a behavioral response form Trichogramma chilonis females. The parasitoids' response varied depending on the growth stage of the plant. Volatiles emitted by sorghum in the vegetative and reproductive stages arrested the parasitoids. T. chilonis females did not respond to volatiles from pigeonpea in the vegetative stage, but were repelled by volatiles from plants in the reproductive stage. Plants in the reproductive stage are preferred for oviposition by H. armigera. Thus, sorghum is attractive and pigeonpea repellent to T. chilonis females at the time when each plant is attractive to the host. This difference in the parasitoids' response may partly explain the different levels of egg parasitism reported from these two crops. The infochemicals involved in these plant–parasitoid interactions are discussed in the context of the current terminology.     

Oviposition response ofLobesia botrana females to long-chain free fatty acids and esters from its eggs

Avoidance of occupied ovisposition sites supposes that females perceive information related to their own progency. Fatty acids identified from egg extracts have been reevaluated using a different extraction method, and we have investigated the dose-dependent oviposition response of European grape vine moths (Lobesia botrana) to myristic acid, palmitic acid, palmitoleic acid, stearic acid, oleic acid, linoleic acid, methyl palmitate, methyl oleate, and ethyl palmitate; all except ethyl palmitate have been identified from eggs ofL. botrana. A methylene dichloride extract of eggs fromL. botrana revealed the presence of saturated free fatty acids (myristic, palmitic, and stearic) and unsaturated acids (palmitoleic, oleic, linoleic, and linolenic) in amounts ranging from 3.9 ng/egg equivalent for myristic acid to 30 ng/egg equivalent for palmitic and oleic acids. The extract also contained traces of methyl palmitate and methyl stearate. The greatest avoidance indexes were observed in response to palmitic, palmitoleic, and oleic acids. All the other compounds tested caused weaker responses. A reduction in the number of eggs laid was observed when moths were exposed to each of the esters applied at 0.3 µg per application spot. Reduction in eggs laid was also observed at a 10-fold higher dose of oleic acid. The present results confirm that general and simple molecules can be involved in the regulation of oviposition site selection and that they may participate in chemical marking of the eggs.     

20-Hydroxyecdysone Deters Oviposition and Larval Feeding in the European Grapevine Moth, Lobesia botrana

European grapevine moth females (Lobesia botrana, Lepidoptera Tortricidae) select an oviposition site by tasting the host plant surface and then gluing a single egg on berries from grapes or from several other host plant species. In doing so, females should avoid ovipositing on plants that are detrimental to their progeny. Do they sense the same deterrent compounds as larvae, despite the fact that they do not have access to the same compartments of the plants? We tested this hypothesis with 20-hydroxyecdysone (20E), purified from Leuzea carthamoides. Phytoecdysteroids are usually found inside plant tissues and accessible to larvae in an aqueous phase, while adults would access them only through the epicuticular wax. We first confirmed that larvae avoid feeding on 20E and that they taste 20E with their lateral sensilla styloconica, at a threshold of 10^?6 M. Then, we tested whether adult females avoid ovipositing on glass spheres sprayed with 20E. When given a choice, females avoided laying eggs on a treated surface, at a threshold of 8 ng/cm². In addition, they deposited significantly fewer eggs in the presence of 20E. Presuming that legs play an important role in assessing the oviposition substrate, we assessed the sensitivity of their taste receptors. In females, 14 taste sensilla are located on the ventral side of the last tarsus of the prothoracic leg. One group of these sensilla house one neuron that is sensitive to 20E, with a detection threshold of about 10^?7 M. The same molecule is thus sensed both in larvae and adults of L. botrana where it respectively inhibits feeding and oviposition.     

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.     

Oviposition Induced Volatile Emissions from African Smallholder Farmers’ Maize Varieties

Maize (corn), Zea mays, is a genetically diverse crop, and we have recently shown that certain open pollinated varieties (OPVs) of Latin American origin possess a trait not present in mainstream commercial varieties: they produce volatiles in response to stemborer oviposition that are attractive to stemborer parasitoids. Here, we tested whether a similar tritrophic effect occurs in the African OPVs ‘Nyamula’ and ‘Jowi’. Herbivore induced plant volatiles (HIPVs) were collected from plants exposed to egg deposition by the stemborer Chilo partellus. In a four-arm olfactometer bioassay, the parasitic wasp Cotesia sesamiae preferred samples containing HIPVs from plants with eggs to samples collected from plants without eggs. EAG-active compounds, including (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), were released in higher amounts from the egg induced headspace samples. Our results suggest that this oviposition trait is not limited to S. American Z. mays germplasm, and that it could be used to increase indirect defense against attack by stemborers.     

Changing Oviposition Preferences of the Desert Locust, Schistocerca gregaria, Suggest a Strong Species Predisposition for Gregarization

Field surveys at five sites within desert locust breeding habitats around Port Sudan during three successive seasons indicated that early in the rainy season the incoming solitary females oviposited predominantly in the vicinity of Heliotropium spp. (66%) and millet (32%) seedlings. Solitary nymphs also preferred to feed on these plants. Follow-up cage experiments were conducted in the field in which solitary and gregarious female locusts were presented with choices of selected desert plants and egg pods. When presented with bulrush millet, Heliotropium spp., Zygophyllum simplex, and untreated moistened sand, solitary females oviposited adjacent to the first two plants (40% and 60%, respectively). However, when offered a choice of either or both of these plants together with egg pods derived from gregarious and/or solitary insects, solitary females showed a significantly higher preference for ovipositing near gregaria egg pods than near the plants, with solitaria egg pods eliciting the least response. In contrast with solitary females and in the absence of gregaria egg pods, gregarious females preferred to oviposit in untreated moist (control) sand (74–77%) away from the plants (6–14%) or solitaria egg pods (4%). However, when present, gregaria egg pods elicited significantly more oviposition. These and previous results indicate a hierarchy of phase-dependent oviposition preferences in the desert locust and are interpreted in terms of a strong propensity of the species to exploit opportunities under appropriate conditions to facilitate congregation and the gregarization of the progeny.     

Identification of Volatile Synomones, Induced by Nezara viridula Feeding and Oviposition on Bean spp., That Attract the Egg Parasitoid Trissolcus basalis

Bean plants (Vicia faba L. and Phaseolus vulgaris L.) damaged by feeding activity of Nezara viridula (L.) (Heteroptera: Pentatomidae), and onto which an egg mass had been laid, produced volatiles that attracted the egg parasitoid Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae). Extracts of volatiles of broad bean and French bean plants induced by adults of N. viridula as a result of their feeding activity, oviposition activity, and feeding and oviposition activity combined were analyzed by gas chromatography-mass spectrometry (GC-MS), and tested in Y-tube olfactometer bioassays as attractants for T. basalis females. In extracts from undamaged leguminous plants, green-leaf volatiles were absent or scarcely detected, and monoterpenes and sesquiterpenes were present at trace levels. No significant differences were detected in the profiles of volatiles of undamaged plants, and undamaged plants on which bugs were allowed only to lay eggs. In contrast, feeding and oviposition by adults of N. viridula induced in both leguminous plants a significant increase in terpenoids such as linalool, (E)-beta-caryophyllene, (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene, and (3E)-4,8-dimethyl-1,3,7-nonatriene, which was induced only in French bean plants. Quantitative comparisons revealed increased levels of (E)-beta-caryophyllene in extracts from feeding-damaged plants with N. viridula egg masses compared to feeding-damaged plants without egg masses. In Y-tube olfactometer bioassays, T. basalis females were attracted by extracts of both leguminous plants only when N. viridula adults were allowed to feed and oviposit upon them. Fractionation of extracts of volatiles from broad bean plants with N. viridula feeding damage and egg masses yielded two fractions. but only the fraction containing (E)-beta-caryophyllene was attractive to the egg parasitoid. These findings indicate that N. viridula feeding and oviposition induce leguminous plants to produce blends of volatiles that are characterized by increased amounts of (E)-beta-caryophyllene, and these blends attract female T. basalis. The role of (E)-beta-caryophyllene as a potential synomone for T. basalis is discussed.     

Evidence for the accessory glands as the site of production of the oviposition attractant and/or stimulant ofLutzomyia longipalpis (Diptera: Psychodidae)

The phlebotomine sandflyLutzomyia longipalpis Lutz and Neiva, the vector of visceral leishmaniasis in South America, has recently been shown to produce an oviposition semiochemical. In the present study it was found that a nonpolar extract of eggs was attractive and/or stimulatory to ovipositing females. A Chromatographic investigation indicated the presence of similar compounds in accessory glands and egg extracts. Extract of accessory gland was also found to elicit a positive oviposition response. It is concluded that the pheromone is produced in the accessory glands and is secreted onto the eggs during oviposition.     

Jasmonic Acid-Induced Changes in <Emphasis Type="BoldItalic">Brassica oleracea</Emphasis> Affect Oviposition Preference of Two Specialist Herbivores

Jasmonic acid (JA) is a key hormone involved in plant defense responses. The effect of JA treatment of cabbage plants on their acceptability for oviposition by two species of cabbage white butterflies, Pieris rapae and P. brassicae, was investigated. Both butterfly species laid fewer eggs on leaves of JA-treated plants compared to control plants. We show that this is due to processes in the plant after JA treatment rather than an effect of JA itself. The oviposition preference for control plants is adaptive, as development time from larval hatch until pupation of P. rapae caterpillars was longer on JA-treated plants. Total glucosinolate content in leaf surface extracts was similar for control and treated plants; however, two of the five glucosinolates were present in lower amounts in leaf surface extracts of JA-treated plants. When the butterflies were offered a choice between the purified glucosinolate fraction isolated from leaf surface extracts of JA-treated plants and that from control plants, they did not discriminate. Changes in leaf surface glucosinolate profile, therefore, do not seem to explain the change in oviposition preference of the butterflies after JA treatment, suggesting that as yet unknown infochemicals are involved.