Abstracts

Publications of Dr. Aijun Zhang

Field tests of predaceous pentatomid pheromones and semiochemistry of Podisus and Supputius species (Hemiptera: Pentatomidae: Asopinae). Return

Traps baited with synthetic pheromones for either Podisus nigrispinus (Dallas) or Supputius cincticeps (St†l) were field tested at the Universidade Federal de Vi‡osa, Minas Gerais, Brazil, beginning September 7, 1995. No P. nigrispinus were caught but, in September and October, several adult males and females of P. distinctus (St†l) were caught along with a few adults of S. cincticeps and two females of a tachinid fly parasitoid, Cylindromyia atra Roeder. Chemical analysis of the pheromone gland extract of P. distinctus males indicated that this species produces a pheromone containing the major compounds of P. nigrispinus and S. cincticeps . Therefore, on November 6 a set of traps was baited with the pheromones of both P. nigrispinus and S. cincticeps, and monitored in the field until February 6, 1996. During this second phase of the study, six times more P. distinctus were caught in the combined pheromone treatment than in traps baited only with the P. nigrispinus pheromone. The phenology of these neotropical asopines is like that for P. maculiventris (Say) in temperate North America, although fewer predators and host-seeking parasitoids were caught. Suspected pheromones were also identified for P. rostralis (St†l) from Goi s, Brazil, and P. sagitta (Fabricius) from Honduras. In addition, the chemistry of other exocrine secretions from these neotropical species was investigated. Armadilhas contendo ferom“nios sint‚ticos de Podisus nigrispinus (Dallas) e Supputius cincticeps (St†l) foram testadas no campo, na Universidade Federal de Vi‡osa, Minas Gerais, Brasil, a partir de 7 de setembro de 1995. Durante a coleta (setembro-outubro/95), nao se observoua presen‡a de P. nigrispinus nas armadilhas em teste. No entanto, diversos adultos (machos e fˆmeas) de Podisus distinctus (St†l) foram coletados durante o mesmo per¡odo, bem como, alguns adultos de S. cincticeps e dois parasit¢ides fˆmeas de Cylindromyia atra Roeder (Diptera: Tachinidae). An lises qu¡micas do extrato glandular de machos de P. distinctus indicaram que os principais compostos feromonais desta esp‚cie, tamb‚m sao produzidos por P. nigrispinus e S. cincticeps . Devido a este fato, em 6 de novembro, foram colocadas no campo uma s¡rie de armadilhas contendo iscas feromonais tanto de P. nigrispinus , como de S. cincticeps . As armadilhas foram monitoradas at‚ 6 de fevereiro de 1996. Durante esta segunda etapa do estudo, observou-se que a combina‡ao das duas iscas feromonais aumentou em seis vezes a coleta de adultos de P. distinctus, em compara‡ao com aquelas onde havia somente a isca para P. nigrispinus . Embora a fenologia para estes asopines neotropicais seja semelhante a do predador norte-americano de clima temperado Podisus maculiventris (Say), menos predadores e parasit¢ides hospedeiros foram coletados. Poss¡veis ferom“nios foram identificados para Podisus rostralis (St†l), em Goi s, Brasil, e Podisus sagitta (Fabricius), de Honduras. Compostos qu¡micos de outras secre‡oes exocrinas destas esp‚cies neotropicais tamb‚m foram estudados.

Status of semiochemical research on predatory Heteroptera. Return

The progress of semiochemical research on terrestrial predatory Heteroptera is reviewed, and new directions for research and the use of predators for biological control are proposed. Pheromones have been identified for several predacious stink bugs (Pentatomidae: Asopinae), and one species of assassin bug (Reduviidae). For another group of important predatory bugs, the Anthocoridae, pheromones have yet to be indentified, but there is considerable evidence that they exploit cues from prey (kairomones) or from plants damaged by prey (synomones) to direct their foraging. The difficulty of implementing exotic species for biocontrol of endemic pests makes managing native beneficials more important. It is proposed that, for augmentative purposes, generalist predators offer the greatest potential for commercialization because of the broad-based market for these biocontrol agents, and the potential for semiochemicals to mitigate the inevitable bottleneck of conventional mass-rearing programs.

Semiochemistry of aposematic seed bugs (Heteroptera: Lygaeidae). Return

(E)-2,7-Octadienyl acetate and (E)-2-octenyl acetate (1:10 by volume) were identified as a pheromone attractive to both sexes of the lygaeid bug, Tropidothorax belogolowi. In a parallel investigation of Neacoryphus bicrucis (Lygaeidae), (E,E)-2,4-hexadienyl acetate and phenethyl acetate (~9:1) were identified from males, and found attractive to both sexes of adults in the field plus a tachinid fly parasitoid of the bugs. In N. bicrucis, the pheromone was clearly shown to come from the tubular accessory glands of the metathoracic scent gland; this evidence, plus earlier literature reports for other species, indicate that male lygaeids are the pheromone emitters. In another lygaeid, Oncopeltus fasciatus, 2- isobutyl-3-methoxypyrazine was identified in the cardiac glycoside-laden fluid sequestered from milkweed hosts and expelled by these bugs when they are attacked. Alkyl methoxypyrazines are warning odorants associated with poisonous insect secretions, and their presence in O. fasciatus indicates that the plant-derived chemical defense of lygaeines is more elaborate than previously appreciated.

Pheromone-induced movement of nymphs of the predator, Podisus maculiventris (Heteroptera: Pentatomidae). Return

Males of the generalist predator, Podisus maculiventris (Say) (Heteroptera: Pentatomidae) (known as the spined soldier bug), attract mates with a pheromone, but the immature stages of the predator also appeared to be attracted. Therefore, attraction of nymphs of P. maculiventris to pheromone was studied in a wind tunnel and in field plots. The behavior of individual nymphs toward pheromone with and without Colorado potato beetles, Leptinotarsa decemilineata (Say) (Chrysomelidae), and/or potato plants in the airstream, was studied in a wind tunnel. Field experiments were performed in plots planted with green beans, Phaseolus vulgaris, that were allowed to become naturally infested with Mexican bean beetles, Epilachna varivestis (Moulsant) (Coccinellidae). Spined soldier bug nymphs were released in the middle row of plots three weeks after planting, and three commercial pheromone dispensers were placed outside the thirteenth row of a plot. Podisus maculiventris nymphs were significantly attracted to synthetic pheromone both in the laboratory and in the field. Results of wind tunnel experiments indicated that combining the pheromone with the phytophage significantly increased the positive responses of nymphs compared to the pheromone alone; however, inclusion of damaged or undamaged potato plants with pheromone did not enhance the positive responses to the odor source. Spined soldier bugs released in field plots remained relatively sedentary for the first day after release, but by the end of the 1- week sampling period nymphs had significantly dispersed into rows nearer the pheromone dispensers. The ability to manipulate immature spined soldier bugs significantly expands the potential for using this generalist predator in integrated pest management programs.

Management of predaceous hemipterans with semiochemicals: Practice and potential. Return

Two ongoing research projects involving predaceous hemipterans will be discussed: 1) pheromone-mediated augmentation of the spined soldier bug (SSB), Podisus maculiventris (Say) (Pentatomidae), for suppression of the Colorado potato beetle (CPB) and, 2) the isolation and identification of the suspected sex pheromone of Orius insidiosus (Say) (Anthocoridae). The SSB overwinters in the adult stage, and a synchronized, massive emergence occurs just prior to the bud burst of deciduous trees in the eastern U. S. The commercialized, male-produced pheromone of this predator (attractive to both sexes and nymphs) is being used to harvest wild adults in pheromone- baited traps to mass-produce and manipulate young predators for augmentative biological control. Results after the second year of a 3-year project indicate that the average potato plant defoliation by the CPB in May was 20% in the plots where the soldier bugs were released (ca. 5 nymphs/plant), and 44% where the bugs were not released (9 potato plots; 500 m2/plot; ca. 1036 plants/plot). The average potato plant in the release plots produced 454g of tubers whereas production in the control plots was 60g, an 87% yield reduction. For Orius insidiosus, Y-tube olfactometer bioassays showed that males are attracted to volatiles from virgin females. Suspected attractants were isolated by whole-body extraction, aeration, and microdissection. Three novel female-specific compounds have been identified: (2E,7)-octadienal, (2E,7)-octadienoic acid, and (2E,9)-decadienal. Further laboratory and field tests are planned to determine if these compounds are attractive to conspecifics.

Biochemistry of the exocrine secretion from gypsy moth caterpillars (Lepidoptera: Lymantriidae: Lymantria dispar (L.)). Return

Gypsy moth caterpillars have unpaired dorsal abdominal glands on the sixth and the seventh segments, and pairs of smaller glands on the first to fourth abdominal segments. Normally, material from these glands becomes sticky and is regularly dispersed onto setae by the caterpillars, but if larvae are held at saturated humidity for 3-4 days, droplets accumulate on the glands and remain fluid. The secretion is an aqueous mixture of low molecular weight molecules including the biogenic amine, gamma-aminobutyric acid, short- chain hydroxy acids (e.g. alpha-hydroxyisobutyric acid), and Krebs cycle acids (e.g. isocitric acid), plus higher molecular weight compounds (>;30,000 MW). 2-Isobutyl-3-methoxypyrazine, considered to be a warning odor in many aposematic insects, also occurs in the secretion in minute amounts (<1 picogram/larva), yet is mainly responsible for the exudate odor which is detectable from individual caterpillars. Natural secretion from L. dispar larvae was a feeding deterrent to foraging fire ants in a laboratory bioassay. All Lymantriidae have dorsal abdominal glands; therefore, it is likely that secretion from these glands contributes to the irritating and allergenic properties associated with setae from tussock moth caterpillars.

Semiochemistry of cabbage bugs (Heteroptera: Pentatomidae: Eurydema and Murgantia). Return

The semiochemistry of the common North American pest of crucifers, Murgantia histrionica (Hahn) (the harlequin bug), and two related European species, Eurydema ventrale L. and E. oleraceum L., was investigated. The metathoracic scent glands of these warningly colored stink bugs (Pentatomidae) are smaller than the scent glands of most cryptically colored pentatomids, and the secretions from the scent glands of Murgantia and Eurydema species include two heretofore unknown natural products: (2E,6E)-octadienedial and (2E,6E)- octadiene-1,8-diol diacetate. It was also discovered that when harlequin bug adults are squeezed, they expel a frothy fluid from the margins of the prothorax with a distinctive odor due to the presence of 2-sec -butyl- 3-methoxypyrazine and 2-isopropyl-3-methoxypyrazine. The presence of alkylmethoxypyrazines in the expelled fluid of harlequin bugs extends the known distribution of these compounds to include the Heteroptera, and strengthens the argument that this class of pyrazines constitute a universal warning odor equivalent to the color red as a visual warning signal.

Identification of the presumed pheromone blend from the Australasian predaceous bug, Oechalia schellenbergii (Heteroptera:Pentatomidae). Return

Oechalia schellenbergii is one of the most common predatory insects in Australia, and islands of the South Pacific. Adult males of this predaceous "true bug" collected during March near Gatton, Queensland, Australia, had a pair of enlarged exocrine glands opening underneath their wings that presumably produce an attractant pheromone. The two major components of the secretion are 3-methylenehexyl acetate and 9-hydroxygeranyl diacetate (2,6- dimethyl-2(E),6(E)-octadien-1,8-diol diacetate).

Testing the New Associations biological control concept with a tachinid parasitoid (Euclytia flava). Return

Males of the spined soldier bug, Podisus maculiventris (Heteroptera: Pentatomidae), produce an attractant pheromone that is exploited as a host- finding kairomone by a complex of parasitic species. The capability to catch hundreds of a generalist tachinid fly parasitoid, Euclytia flava, alive in traps baited with the pheromone of P. maculiventris provided an opportunity to test the premise of the new associations biological control concept (Hokkanen and Pimentel, 1989). The hypothesis that host species newly associated with a parasitoid are maladapted relative to native-native associations was tested by giving E. flava females a choice between native and exotic stink bugs (Heteroptera: Pentatomidae). Wild E. flava females preferred to oviposit on exotic pentatomid species rather than indigenous, known host species, both in field traps baited with the pheromone of a native host and in the laboratory. Data presented here demonstrate that an invader may be vulnerable to native parasitoids in one aspect of the parasitism process (acceptance), yet go unrecognized as a potential host.

Flight-mediated attraction of Biprorulus bibax Breddin (Hemiptera: Pentatomidae) to natural and synthetic aggregation pheromone. Return

The attraction of female spined citrus bugs, Biprorulus bibax, to natural and synthetic aggregation pheromone was studied using an olfactometer and a large flight cage. No locomotory response by postdiapause, prereproductive females to heptane extracts of male dorsal abdominal glands (DAGs) (site of pheromone production) was recorded in the olfactometer study. However, postdiapause, prereproductive females showed significant attraction to sites baited with DAG extracts in the flight cage (1.9-3.0 times that of unbaited sites). Prereproductive and reproductive females showed greatest attraction to sites baited with a synthetic blend of pheromone ((3R,4S,1'E)-3,4-bis(1'-butenyl)tetrahydro-2-furanol, linalool, farnesol, nerolidol) (2.3-4.7 times the attraction of unbaited sites). Females also responded significantly to sites baited with the hemiacetal major component alone (1.7-2.2 times ). Diapausing females collected from fall populations did not respond to natural or synthetic pheromone baits. Potential applications of the synthetic aggregation pheromone are discussed with respect to B.

Identification, synthesis and bioactivity of a male-produced aggregation pheromone in the assassin bug, Pristhesancus plagipennis (Hemiptera: Reduviidae). Return

Pristhesancus plagipennis, a large Australian assassin bug, possesses three pairs of dorsal abdominal glands (DAGs). In the male, the anterior and posterior glands are hypertrophied and secrete an attractant pheromone. Gas chromatography-mass spectrometry (GC-MS) analyses of male DAG extracts and airborne volatiles emitted from calling males showed the pheromone signature to be dominated by a novel component. Subsequent chemical manipulations. GC- MS, and chiral-column analyses established its identity as (Z)-3- hexenyl (R)-2-hydroxy-3-methylbutyrate. Minor components included 3- methylbutanol, 2-phenylethanol, (Z)-3-hexenol, decanal, (E)-2-hexenoic acid, and three minor hexenyl esters. Bioactivity studies using laboratory olfactometers and outdoor flight cages demonstrated attraction by female P. plagipennis to calling males, heptane extracts of male posterior DAGs and a synthetic formulation of the (Z)R enantiomer of the major ester, alone or in combination with other components of male anterior and posterior DAGs. Males were also attracted to the major ester. The racemate and S enantiomer of the ester were not attractive. Contamination of the (Z)R enantiomer with 30-60% of the E isomer also made the compound nonattractive. This is the first report of an aggregation pheromone in the Reduviidae. The prospects for pheromonal manipulation of P. plagipennis populations to enhance the value of this predator in horticultural ecosystems, are discussed.

Identification of male-specific volatiles from Nearctic and Neotropical stink bugs (Heteroptera: Pentatomidae). Return

Males of the Central American stink bug species, Euschistus obscurus, produce an attractant pheromone composed of a blend of compounds characteristic of North American Euschistus spp. and the South American soybean pest, E. heros. The range of E. obscurus extends into the southern U. S., the species is easy to rear, and males produce an exceptionally large quantity of pheromone (>0.5 mg/day/male). These factors made E. obscurus useful for characterizing the novel pheromone components of E. heros without importing this pest species into the U. S. Euschistus obscurus males produce methyl (2E,4Z)- decadienoate (61%) in abundance, which is characteristic of North American species, and methyl 2,6,10-trimethyltridecanoate (27%), the main male-specific ester of E. heros. The chirality of Euschistus spp. methyl- branched esters, and field activity of synthetic formulations, remain to be determined.

Male-specific volatiles from Nearctic and Australasian true bugs (Heteroptera: Coreidae and Alydidae). Return

Aeration and exocrine gland extracts were analyzed for three Coreidae and two Alydidae. Males of all the species studied emit volatile blends that are probably pheromones, but sexual communication in these insects evolved differently. In the alydids, Riptortus serripes and Mirperus scutellaris, the metathoracic scent glands are sexually dimorphic, and the dimorphisms are expressed chemically. Secretions from the male alydids contain high concentrations of esters or alcohols (e.g. (E)-2-hexenyl (Z)-3-hexenoate, (E)-2-hexenyl butyrate, and (E)-2- octenol), while females produce mainly acids and aldehydes (e.g. butyric and hexanoic acids, and (E)-2-hexenal). In the coreids, Amblypelta lutescens lutescens, Amblypelta nitida and Leptoglossus phyllopus, the metathoracic scent glands are not sexually dimorphic, but male- and species-specific volatiles are released, apparently from cells in the cuticular epidermis. The coreid male-specific volatiles are primarily monoterpenes and sesquiterpenes, including (-)-(3R)-(E)-nerolidol as the major component from A. lutescens lutescens (an Australasian species) and L. phyllopus (a Nearctic species). Only (+)-(3S)- (E)-nerolidol is commonly found in plants, so (E)-nerolidol from these coreids is environmentally unique because of its chirality.

Artifacts and pheromone blends from Nezara spp. and other stink bugs (Heteropera: Pentatomidae). Return

Isomeric compounds reportedly released by mature males of Nezara viridula as attractants for conspecific females are evidently artifacts formed by dimerization of (E)-4-oxo-2-hexenal. Additional analyses of the male-specific volatiles from Italian, Australian, Brazilian, and Japanese populations of N. viridula verify that at least two distinctive pheromone strains exist, but an active synthetic pheromone has not yet been developed. Analyses of volatiles from N. antennata and Acrosternum aseadum males are also reported showing that the native Japanese Nezara sp., and species in the sister genus Acrosternum, produce species-specific blends based on the same compounds as N. viridula: (Z)-alpha-bisabolene (1-methyl-4-(1,5-dimethyl-(Z)-1,4- hexadienyl)-cyclohexene), and trans- and cis-1,2-epoxides of (Z)-alpha-bisabolene. The trans-/cis-1,2-epoxide ratio of N. antennata is within the range found for most N. viridula populations, but the blend from Japanese N. viridula males deviates radically from those of other conspecific populations.

A long range attractant kairomone for the egg parasitoid Trissolcus basalis, isolated from the defensive secretion of its host, Nezara viridula. . Return

A short-chain alpha,beta-unsaturated aldehyde, (E)-2-decenal, present in the defensive metathoracic gland of containing adult N. viridula, but we also found that female T. basalis would examine and probe glass beads coated with an acetone extract of the metathoracic gland from males or females. Using this bioassay, the kairomone was isolated by bioassay directed by preparative gas chromatography and identified by NMR and mass spectrometry as (E)-2-decenal. The biological activity of the identified aldehyde was compared with analogs to determine specificity. An unstable Z isomer was found to be more active but not present in detectable or behaviorly relevant levels in the host, based on the bell-shaped dose-response curve of the two isomers. An investigation was also designed to determine if the E isomer was also responsible for the egg recognition kairomone activity previously reported. However, no 2- decenal isomers were detected in host egg extracts and the chemical characteristics of