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.     

Host-specific recognition kairomone for the parasitoidMicroplitis croceipes (Cresson)

A water-extractable host recognition kairomone in frass of corn earworm,Helicoverpa zea Boddie (Lepidoptera: Noctuidae), host larvae stimulates antennation by females of the parasitoidMicroplitis croceipes Cresson (Braconidae: Hymenoptera). In addition, when the wasps contact water extracts of host frass they will subsequently fly in a flight tunnel to odor associated with the extract. Contact with water extracts of cowpea leaves or with water extracts of frass from larvae of nonhost beet armyworm, fall armyworm, or cabbage looper that were fed cowpea leaves does not stimulate antennation, nor do wasps fly to associated odors after contact with these substances. However, contact with the water extract of host frass in association with hexane extract of cowpea-fed nonhost frass will induce the wasps to subsequently fly to the hexane extract of the nonhost frass when it is used as an odor source in a flight tunnel. Thus the host-specific kairomone by whichM. croceipes recognizes the frass of its host is extractable with water. This substance plays a crucial role in the foraging behavior of this parasitoid by allowing it to recognize host frass and to learn to search for odors originating from plants on which the host is feeding.     

Role of host-produced stimuli and learning in host selection behavior ofCotesia (=Apanteles) marginiventris (Cresson)

The study was conducted to determine how various factors, including learning, influence the host-selection behavior of the larval parasitoid Cotesia (=Apanteles)marginiventris (Cresson). Frass, silk, and feeding damage fromSpodoptera frugiperda (J.E. Smith) larvae elicited visits and antennal examinations by females of the parasitoid. Learning played a role in the effective response to these stimuli in that previous contact experience with hosts and/or chewed leaves, exuviae, frass, or hemolymph significantly enhanced the response of the parasitoid. Previous contact with host plants alone did not improve the responses. Experienced parasitoids were more active and spent less time at rest than inexperienced parasitoids. Previous experience was also found to be of significant importance in the ability of the parasitoid to discriminate between parasitized and unparasitized host larvae.Hymenoptera: Braconidae.In cooperation with the University of Georgia College of Agriculture Experiment Stations, Coastal Plain Station, Tifton, Georgia 31793-0748.Mention of a proprietary product in this paper does not constitute endorsement of this product by the USDA.Visiting scientist with the Department of Entomology, Coastal Plain Station, Tifton, Georgia, during this study.     

Sources of fall armyworm,Spodoptera frugiperda (Lepidoptera: Noctuidae), kairomones eliciting host-finding behavior inCotesia (=Apanteles) marginivenitris (Hymenoptera: Braconidae)

Bioassay responses inCotesia marginiventris (Cresson) females to materials derived from fall armyworm (FAW) larvae,Spodoptera frugiperda (J. E. Smith), were most intense for frass and somewhat less intense for larval and pupal cutical materials, scales, exuviae, silk, and oral secretion, with FAW larval hemolymph eliciting only a slight response. The highest percentage of ovipositor probing was caused by frass (100%) and moth scales (90%). Various types of corn-leaf damage when assayed alone did not produce responses as intense as when assayed in combination with frass, cuticle material, and oral secretion. Parasitoid response was somewhat better to frass derived from FAW larvae feeding on corn and peanut leaves than from larvae feeding on the foliage of soybeans, Bermuda grass, cowpeas, or laboratory diet. Hexane and chloroform were better than methanol and water for extracting active material from FAW frass, and chloroform was the best of these solvents for extracting corn leaves. Serial dilutions of frass extracts resulted in a reduction in parasitoid response.This paper was submitted in partial fulfillment of the requirements for Doctor of Philosophy, Department of Entomology and Nematology, University of Florida, Gainesville.     

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

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

Attraction of Dibrachys cavus (Hymenoptera: Pteromalidae) to its Host Frass Volatiles

The European grapevine moth, Lobesia botrana (Lepidoptera: Tortricidae), is a polyphagous insect able to develop on grapes and wild plants. We tested the hypothesis that the parasitoid Dibrachys cavus (Hymenoptera: Pteromalidae) uses the larval frass in its host search. A two-armed olfactometer was used to measure the attractiveness of L. botrana larvae, their silk, or their frass after larvae were fed on different host plants. Frass of three Lepidoptera (L. botrana, Eupoecillia ambiguella, Sphinx ligustri) and one Orthoptera (Chorthippus brunneus) was assayed, but only L. botrana was used to test an effect of the larval host plant (two grape cultivars and three other plant species) to D. cavus females. Larvae without frass did not attract D. cavus whatever their origin, but their frass was attractive at a dose of 2–3 days equivalent of larval frass production. The silk produced by a single larva (L. botrana) was not attractive to D. cavus. The parasitoid was most attracted to the odor of S. ligustri; the frass of L. botrana was more attractive than that of E. ambiguella, irrespective of the species on which D. cavus had been reared. There was no difference in attractiveness of frass collected from L. botrana raised on food containing different plants. Chemical extracts using five different polarity solvents (acetone, dichloromethane, hexane, methanol, and water) differed in attractiveness to D. cavus. Water and dichloromethane were the most attractive. This suggests that a complex volatile signal made from intermediate to polar volatiles may be involved in attraction. D. cavus used frass to discriminate between different potential host species. Our results revealed that the larval food of L. botrana did not modify frass attractiveness, but that the moth species did.     

Beneficial arthropod behavior mediated by airborne semiochemicals. II. Olfactometric studies of host location by the parasitoidMicroplitis croceipes (Cresson) (Hymenoptera: Braconidae)

The response ofMicroplitis croceipes (Cresson) to odors from a plant-host complex was investigated using a four-choice olfactometer. Female, but not male, parasitoids responded in a dose-dependent fashion to volatiles from the plant-host complex and oviposition experience enhanced this response. Female age had no apparent effect on the response. Both artificially damaged leaves and frass elicited positive responses but of lower magnitude than those elicited by the plant-host complex. Volatiles collected from the plant-host complex placed on filter paper also elicited positive responses by female parasitoids.Mention of a commercial or proprietary product does not constitute an endorsement by the USDA.     

Beneficial arthropod behavior mediated by airborne semiochemicals

Heliothis zea (Boddie) larvae fed cowpea seedlings produced volatile semiochemicals to whichMicroplitis demolitor Wilkinson responded in a wind tunnel. However, mostM. demolitor females reared fromH. zea larvae fed an artificial diet were not responsive at emergence to the same volatile semiochemicals. A preflight contact with frass fromH. zea fed cowpea was needed to stimulate a response of sustained flight in a wind tunnel. The most consistent flight response was 7–10 days postemergence. Response resulting from both antennal and ovipositor contact with host frass during preflight stimulation was no better than from antennal contact alone. Chilling the parasitoid pupae rendered most of the emerging females unresponsive to volatile semiochemicals.Hymenoptera: Braconidae.     

Mechanisms of behavioral alterations of parasitoids reared in artificial systems

A high quality of mass reared parasitoids is required for successful biological control of pest insects. Although the phenomenon of behavioral deterioration of parasitoids due to rearing in artificial conditions is well known, its significance is often underestimated, and the underlying mechanisms are poorly investigated. We quantified behavioral alterations of parasitoids reared in an artificial system vs. a natural system and elucidated some of the mechanisms involved. The model systems consisted of apple fruits (natural system) or an artificial diet devoid of apple (artificial system), the herbivore Cydia pomonella, and its larval parasitoid Hyssopus pallidus, a candidate biological control agent. Two parasitoid strains, one reared for 30 generations in the natural system and one in the artificial system, were compared by using the females' ability to respond to frass from codling moth caterpillars fed on apple fruits (apple-frass). The searching response of parasitoids reared in the artificial system compared to those reared in the natural system was reduced by an average of 53.2%. Gas chromatography–mass spectrometry (GC-MS) analyses of the two types of caterpillars' food and of the two corresponding types of frass showed that 15 compounds were present only in apple fruits and apple-frass, three compounds only in artificial diet and artificial-diet-frass, while four compounds were present in both frass types but not in the food sources. This suggests the presence of a food-derived and a host-derived component in the frass. Results from both bioassays and chemical analyses indicate that the kairomonal activity of the frass is due to both apple fruit and host components. The reduced response of parasitoids reared in artificial conditions might, therefore, be due to a lack of recognition of the apple fruit component. In a further experiment, the two parasitoid strains were reared in the opposite system for one generation. While the response to the host frass was significantly reduced in parasitoids that emerged from the artificial system, it was fully restored in parasitoids that emerged from the natural system. This indicates that the behavioral alteration was related to a learning process during ontogenesis rather than to a selection exhibited over generations.     

Investigation of oviposition deterrent in larval frass ofSpodoptera littoralis (Boisd.)

Previous experiments demonstrated an oviposition-deterring effect of larval frass in the Egyptian cotton leaf worm,Spodoptera littoralis (Boisd.). In this study, females were shown to perceive the oviposition-deterring substance(s) with their antennae. During dark, airtight, and cold (–10 °C) storage, the deterrent was persistent for at least 395 days. On the other hand, larval frass retained its activity for only two days when applied to cotton leaves. The deterrent activity of frass was independent of larval density. Frass of larvae reared at high densities deterred oviposition as well as frass of larvae feeding separately or in small groups. For significant oviposition deterrence, the minimum amount of frass was in the range of 5–10 mg frass per cotton leaf. An acetone extract of larval frass was highly deterrent, in contrast to extracts prepared with water, ethanol, chloroform, or pentane.     

Kairomones and their use for management of entomophagous insects

Data are presented that demonstrate the responsiveness ofChrysopa carnea Stephens larvae to kairomones in the moth scales ofHeliothis zea (Boddie). Rates of predation byC. carnea on eggs ofH. zea were increased whenH. zea moth scales or a hexane extract of the scales was applied to the search area under laboratory and greenhouse conditions.Lepidoptera:NoctuidaeNeuroptera:ChrysopidaeIn 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 of this product by the USDA.     

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

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

Host location inOlesicampe monticola,a parasite of larvae of larch sawflyCephalcia lariciphila

In the laboratory, ovipositor probing in mated femaleOlesicampe monticola was elicited by freshCephalcia lariciphila frass but not by aged frass or freshly spun larval silk. Second instar sawfly larvae andLarix needles also elicited a low level of ovipositor probing. Extracts of frass in dichloromethane, but not hexane, were also active. No difference in response was found to frass fromC. lariciphila larvae fed on three varieties ofLarix, (L. kaempferi, L. decidua andL. × eurolepis).     

Volatile fatty acids of frass of certain omnivorous insects

The frass of the following omnivorous insects reared on natural and artificial diets was analyzed for volatile fatty acids:Blattella germanica, Acheta domesticus, Blaberus discoidalis. Acetic, propionic, isobutyric, butyric, isovaleric, and valeric acids were identified in all frass samples. The possible significance of volatile fatty acids in frass is discussed.     

Plant-natural enemy association in the tritrophic system,Cotesia rubecula-Pieris rapae-brassiceae (cruciferae): I. Sources of infochemicals

The role of airborne infochemicals in host selection by the parasitoidCotesia rubecula (Marshal) (Hymenoptera: Braconidae) was examined in a wind tunnel. To elucidate the role of volatile chemicals in attractingC. rubecula to cabbage infested by the host [Pieris rapae L. (Lepidoptera: Pieridae)], the potential sources of volatiles related toP. rapae infestation on cabbage were tested individually. The responses of females to nonhost plant species, bean and geranium, as well as to frass of a nonhost lepidopteran were also examined.C. rubecula was attracted to cabbage previously infested byP. rapae and to frass and regurgitate ofP. rapae. No attraction was observed to larvae ofP. rapae alone. Females were also attracted to mechanically damaged cabbage, cabbage previously infested byPlutella xylostella L. (Lepidoptera: Plutellidae) (a nonhost lepidopteran herbivore), and cabbage previously infested by snails (a nonhost, noninsect herbivore). Intact cabbage, bean, and geranium plants elicited no attraction. A low frequency of attraction was observed to mechanically damaged bean and geranium. Attraction was also observed to frass ofP. xylostella. Volatiles from cabbage related to damage, and volatiles from frass and regurgitate of the host seem to play an important role in guidingC. rubecula to plants infested by its host.     

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.     

Chemical and ultrastructural analysis of corn cuticular lipids and their effect on feeding by fall armyworm larvae

The cuticular lipid composition of lower and upper leaves of five genotypes of field-grown corn,Zea mays L., was determined by combined gas chromatography-mass spectrometry. Surface lipids of the upper leaves had a higher proportion ofn-alkanes (45–52%) than the lower leaves, while the lower leaves had higher percentages of fatty alcohols (12–18%) than the upper leaves. Scanning electron microscopy showed that the upper leaves of two corn genotypes, MpSWCB-4 and Cacahuacintle X's, had a smooth amorphous appearance, while the lower leaves had a dense array of wax crystals.Spodoptera frugiperda (J.E. Smith) larvae weighed more and developed more rapidly when they were reared on diet containing corn foliage from which the cuticular lipids had been removed than when they were fed untreated foliage. However, growth was not inhibited when larvae were fed diet containing the cuticular lipid extracts or individual cuticular lipid components.     

Fate of iridoid glycosides in different life stages of the Buckeye,Junonia coenia (Lepidoptera: Nymphalidae)

The buckeye butterfly,Junonia coenia (Lepidoptera: Nymphalidae), specializes on plants that contain iridoid glycosides. To determine the fate of these compounds in larvae, pupae, and adults of this species, we reared larvae on artificial diets with and without iridoid glycosides, and on leaves of a host plant,Plantago lanceolata (Plantaginaceae). Quantification by gas chromatography showed that newly molted third-, fourth-, and fifth-instar larvae reared on leaves ofP. lanceolata contained means of 5.13, 2.88, and 6.83% dry weight iridoid glycoside. In contrast, the mean iridoid glycoside concentration of actively feeding fifth-instar larvae was 0.28% dry weight, that of pupae was 0.19% dry weight iridoids, and adults contained no detectable iridoids. Feeding experiments suggested that this reduction in actively feeding larvae was due to the metabolism of iridoid glycosides.P. lanceolata leaves in these experiments contained a mean of 1.00% dry weight iridoid glycoside, with a 2:1 ratio of aucubin to catalpol. Calculation of iridoid consumption and utilization indices showed that larvae fed artificial diets consumed, digested, and sequestered aucubin and catalpol in similar ways. When these indices were calculated for larvae fed leaves ofP. lanceolata, catalpol was sequestered twice as efficiently as aucubin.     

Tolerance to Thiarubrines from Ambrosia chamissonis by the Rare Moth Lasionycta wyatti

The larvae of a rare noctuid moth, Lasionycta wyatti, were found to be associated with the stems and roots of Ambrosia chamissonis, a species found along sandy beaches in western North America. High-performance liquid chromatographic (HPLC) analyses of L. wyatti larvae and their frass revealed significant amounts of thiarubrines, secondary compounds characteristic of this host plant. Artificial diet studies showed that thiarubrines were well tolerated by these larvae. These same diets, however, were toxic to larvae of Manduca sexta and inhibited larval growth of Spodoptera litura. Even in the presence of simulated sunlight, artificial diets containing thiarubrines did not affect larvae of L. wyatti. However, dietary incorporation of thiophenes, natural UV-activated breakdown products of thiarubrines, was deleterious to larvae of L. wyatti.     

Iridoid glycosides ofChelone glabra (Scrophulariaceae) and their sequestration by larvae of a sawfly,Tenthredo grandis (Tenthredinidae)

Analysis ofChelone glabra (Scrophulariaceae) by gas chromatography showed that leaves of this plant contained primarily the iridoid glycoside catalpol, and in a few individuals some aucubin was also detected. There was no difference in the iridoid glycoside content of damaged compared to undamaged plants, nor was there a difference between plants collected from a population in Leverett, Massachusetts, and those from plants in an experimental garden in Cambridge, Massachusetts. Larvae and prepupae of the sawfly,Tenthredo grandis (Tenthredinidae) contained catalpol sequestered from the larval host plant. The exuvia also contained catalpol, whereas the frass contained only aucubin. These results indicate that larvae of this sawfly selectively sequester catalpol, eliminating the aucubin in the frass.