Volatiles from Ficus hispida and Their Attractiveness to Fig Wasps

Volatile compositions of receptive (ready to be pollinated), postpollinated, and postparasitized figs, and leaves of Ficus hispida were analyzed. Differences among them were examined, and the specificity of fig wasp attractiveness was investigated. Linalool was the major constituent of steam-distilled oil of either male or female receptive figs, while dibutyl phthalate was the major compound of the oils of postparasitized and postpollinated figs. In petroleum ether extracts, palmitic oil, and 9,12-octadecadienoic acid were the main constituents of male and female receptive figs, while hexadecanoic acid ethyl ester was the major compound of postparasitized and postpollinated figs. In dichloromethane extracts, linalool was the major constituent of male and female receptive figs, 1-hydroxylinalool was the major component of male postparasitized figs, and 1-hydroxylinalool and benzyl alcohol were the major constituents of female postpollinated figs. Bioassays with sticky traps showed that Ceratosolen solmsimarchal was attracted to dichloromethane extracts of male and female receptive figs and to petroleum ether extracts of female receptive figs, but was not attracted to dichloromethane and petroleum ether extracts of male postparasitized and female postpollinated figs. Figs were attractive to pollinating wasps only at the receptive stage. The volatile constituents of receptive figs were different from those of postpollinated or postparasitized figs. From a receptive to a postpollinated state, figs changed in their volatile composition. Some compounds disappeared or decreased in amount. These include linalool, linalool oxide, -terpeneol, and 2,6-dimethyl-1,7-octadiene-3,6-diol, which may act as the attractants of the wasps. Others increased in amount, or several additional chemicals appeared. These include dibutyl phthalate, 1-hydroxylinalool, and benzyl alcohol, which may be repellents of the wasps. That dichloromethane extracts of male and female receptive figs showed similar activities in attracting fig wasps indicates that receptive figs of both sexes are similarly attractive to fig wasps, which is further supported by their similar volatile composition. Leaf extract was not attractive to the wasps.     

Responses of the Pollinating Wasp Ceratosolen solmsi marchali to Odor Variation Between Two Floral Stages of Ficus hispida

During development of figs on Ficus hispida, only the female floral stage is receptive to its pollinator Ceratosolen solmsi marchali. After this stage, the quantity of fig odor decreases. The effects of F. hispida volatiles from receptive figs (figs at the female floral stage, when they are pollinated) and interfloral figs (between the female floral and male floral stages) on their pollinator were studied, together with responses to compounds present in the odor. Odors emitted by both receptive and interfloral figs were attractive to the pollinator. However, wasps preferred the odor of receptive figs to that of interfloral figs even though the quantity of interfloral volatiles increased. Three monoterpenes that included linalool (major constitutent) and two minor compounds limonene and β-pinene from the receptive fig volatiles were used to test the pollinator responses. The levoisomer and racemic mixtures of linalool were attractive to the pollinator at high doses, but the dextroisomer was neutral. (±)-Limonene and (−)-β-pinene at high doses were even less attractive to the pollinator than clean air and were neutral at low doses, while (R)-(+)-, (S)-(−)-limonene were neutral at all doses. In blend tests, all four mixtures of (±)-linalool or (S)-(−)-linalool combined with (±)-limonene or (−)-β-pinene attracted C. solmsi marchali when administered at high doses. (R)-(+)-linalool and (−)-β-pinene enhanced the attractiveness of (S)-(−)-linalool to the pollinator, while enantiomers of limonene did not. These results suggest that both quality and quantity of fig volatiles regulate C. solmsi marchali response and that quality is the main host-finding and floral stage-distinguishing cue for the pollinator. Synergistic effects of some compounds may play a role in enhancing attractiveness of the active compounds.     

Specific Attraction of Fig-Pollinating Wasps: Role of Volatile Compounds Released by Tropical Figs

Floral scents often act as pollinator attractants. In the case of obligate and specific plant–pollinator relationships, the role of floral signals may be crucial in allowing the encounter of the partners. About 750 Ficus species (Moraceae) are involved in such interactions, each with a distinct species of pollinating wasp (Chalcidoidea, Agaonidae). Several species have been shown to release volatile compounds, but their role in pollinator attraction has rarely been simultaneously tested. We investigated the floral scents of four tropical fig species and combined chemical analysis with biological tests of stimulation of insects. Pollinators of three species were stimulated by the odor of their associated fig species and generally not by the odor of another species. The fourth actually comprised two distinct varieties. The main compound was often a different one in each species. Floral blends of different species always shared compounds, but ratios of these compounds varied among species.     

Nest Paper Absorbency,Toughness, and Protein Concentration of a Native vs. an Invasive Social Wasp

The amount of proteinaceous food that was allocated to nest construction by a native wasp (Polistes fuscatus) vs. an invasive wasp (Polistes dominulus) in North America was examined following a field experiment under natural and surplus prey foraging conditions. Wasps of the surplus prey foraging conditions were provided with prey ad libitum within an enclosed area, while wasps of the natural treatment foraged in an adjacent field-woodland site. At the end of the field experiment, each nest was tested for water absorbency, toughness, and protein concentration. The hypotheses were: (1) When all nests are equally sheltered, the invasive P. dominulus (PD) allocates less protein to nest paper construction (for waterproofing and strengthening) and more protein to developing larvae than the native P. fuscatus (PF). (2) Nests of P. dominulus are more absorbent (less waterproof) and less tough than nests of P. fuscatus. Results indicate that P. fuscatus nests from surplus prey foraging conditions were more absorbent (less waterproof) to artificial rain drops than P. dominulus nests. The toughness of nests was similar between wasp species. However, nests from the natural treatment were tougher than those from the surplus prey treatment. Nests from the natural foraging conditions had half as much protein as those from surplus prey foraging conditions. There was no correlation between nest protein concentration and the number of prey taken, the number of cells, the number of adult offspring produced, or the total wasp biomass produced per colony. For PF under surplus prey conditions, protein concentration and absorbency were negatively correlated, but for PD the correlation was positive. In conclusion, when prey were scarce, Polistes wasps allocated less protein to nest construction. Also, the introduced P. dominulus may increase production of offspring by allocating less to nest construction than that of the native P. fuscatus, and so more protein to offspring production.     

Beneficial arthropod behavior mediated by airborne semiochemicals. IX. Differential response ofTrichogramma pretiosum,an egg parasitoid ofHeliothis zea,to various olfactory cues

The behavior ofTrichogramma pretiosum Nixon wasps when exposed to different olfactory cues was studied in a wind tunnel. Compared to clean air, the sex pheromone of its hostHeliothis zea (Boddie) increased wasp residence times, walking times, and path lengths on a platform and decreased walking velocity. If wasps were released on top of a glass rod above a platform, the odor caused the wasps to land shortly after takeoff. In addition, a clear dose effect with regard to total residence and walking times was found. These responses were not elicited by three dosages of the sex pheromone ofSpodoptera frugiperda (J.E. Smith) or by a blend of saturated acetates. These results correspond with the observation thatH. zea is a common field host ofT. pretiosum, whereas eggs ofS. frugiperda are rarely attacked by this parasitoid.     

Discovery and Development of Chemical Attractants Used to Trap Pestiferous Social Wasps (Hymenoptera: Vespidae)

Chemical attractants for trapping temperate social wasps have been discovered during the screening of chemicals as attractants for flies, the study of pentatomid bug pheromones, and the testing of volatiles of fermented sweet baits. Wasp attraction to these chemicals seems to be related to either food-finding or prey-finding behavior. Of these attractive chemicals, commercial lures marketed in North America for trapping wasps generally contain heptyl butyrate, or the combination of acetic acid and 2-methyl-1-butanol. Heptyl butyrate is a very good attractant for two major pest wasp species in North America and minor wasp pests in the Vespula rufa species group. The combination of acetic acid with isobutanol attracted nearly all North American pest species of social wasps, including yellowjackets (Vespula and Dolichovespula), a hornet (Vespa crabro), and several paper wasps (Polistes spp.). The testing of wasp chemical attractants in different geographic areas demonstrated responses of many wasp taxa and showed a broad potential scope for the marketing of trap lures. Comparisons of compounds structurally similar to isobutanol revealed similar activity with 2-methyl-1-butanol, which is now used commercially because of a vapor pressure that is more favorable than isobutanol for formulations and dispensers. Doses and concentrations needed for good wasp catches were determined for heptyl butyrate, acetic acid, isobutanol, and 2-methyl-1-butanol, either formulated in water or dispensed from a controlled release device. Trap designs were developed based on consumer considerations; visual appeal, ease and safety of use, and low environmental impact. The resultant lures and traps are marketed in numerous physical and on-line retail outlets throughout the United States and southern Canada.     

History Matters: Oviposition Resource Acceptance in an Exploiter of a Nursery Pollination Mutualism

In the fig–fig wasp nursery pollination system, parasitic wasps, such as gallers and parasitoids that oviposit from the exterior into the fig syconium (globular, enclosed inflorescence) are expected to use a variety of chemical cues for successful location of their hidden hosts. Behavioral assays were performed with freshly eclosed naive galler wasps. Syconia with different oviposition histories, i.e. with or without prior oviposition, were presented to wasps in no-choice assays and the time taken to the first oviposition attempt was recorded. The wasps exhibited a preference for syconia previously exposed to conspecifics for oviposition over unexposed syconia. Additionally, syconia exposed to oviposition by heterospecific wasps were also preferred for oviposition over unexposed syconia indicating that wasps recognise and respond to interspecific cues. Wasps also aggregated for oviposition on syconia previously exposed to oviposition by conspecifics. We investigated chemical cues that wasps may employ in accepting an oviposition resource by analyzing syconial volatile profiles, chemical footprints left by wasps on syconia, and syconial surface hydrocarbons. The volatile profile of a syconium is influenced by the identity of wasps developing within and may be used to identify suitable host syconia at long range whereas close range preference seems to exploit wasp footprints that alter syconium surface hydrocarbon profiles. These cues act as indicators of the oviposition history of the syconium, thereby helping wasps in their oviposition decisions.     

Chemical Ecology of Fruit Bat Foraging Behavior in Relation to the Fruit Odors of Two Species of Paleotropical Bat-Dispersed Figs (<Emphasis Type="Italic">Ficus hispida</Emphasis> and <Emphasis Type="Italic">Ficus scortechinii</Emphasis>)

We investigated the fruit odors of two bat-dispersed fig species in the Paleotropics, in relation to the foraging behavior of fruit bats, to test the following hypotheses: 1) fruit odor plays a critical role for detection and selection of ripe figs by fruit bats; 2) bat-dispersed fig species are characterized by the same, or similar, chemical compounds; and 3) total scent production, in bat-dispersed figs, increases when fruits ripen. We performed bioassays to test the effect of both natural and synthetic fig fruit odors on the foraging behavior of the short-nosed fruit bat (Cynopterus brachyotis)—an important disperser of figs within the study area. Fruit bats responded to both visual and chemical (olfactory) cues when foraging for figs. However, the strongest foraging reaction that resulted in a landing or feeding attempt was almost exclusively associated with the presence of a ripe fruit odor—either in combination with visual cues or when presented alone. Fruit bats also used fruit odors to distinguish between ripe and unripe fruits. By using gas chromatography (GC) and GC/mass spectrometry (MS), a total of 16 main compounds were identified in the ripe fruit odor of Ficus hispida and 13 in the ripe fruit odor of Ficus scortechinii—including alcohols, ketones, esters, and two terpenes. Additional compounds were also recorded in F. hispida, but not identified—four of which also occurred in F. scortechinii. Total scent production increased in both species when fruits ripened. Both natural and synthetic fruit odors resulted in feeding attempts by bats, with no feeding attempts elicited by unscented controls. Reaction rates to natural fruit odors were higher than those to synthetic blends.     

Mandibular gland allomones ofDasymutilla occidentalis and other mutillid wasps

The mandibular gland secretion of the mutillid wasp,Dasymutilla occidentalis, possesses three short-chained ketones-4-methyl-3-heptanone (4MH), 4,6-dimethyl-3-nonanone (4,6DMN), 4,6-dimethyl-3-octanone (4,6DMO)—and several unidentified compounds. This is the first report of 4,6DMN as a natural product and its synthesis is described. These ketones, which are either known to be ant alarm pheromones or are structurally very similar to ant alarm pheromones, appear to function as allomones against ants, major potential predators of mutillid wasps. The major secretory component, 4-methyl-3-heptanone, which was identified in females and/ or males of the species analyzed within the generaDasymutilla, Timulla, Traumatomutilla, andPappognatha, appears to constitute a chemical character of the defensive secretions of these genera.     

Host Suitability Affects Odor Association in <Emphasis Type="Italic">Cotesia marginiventris</Emphasis>: Implications in Generalist Parasitoid Host-Finding

Insect herbivores often induce plant volatile compounds that can attract natural enemies. Cotesia marginiventris (Hymenoptera: Braconidae) is a generalist parasitoid wasp of noctuid caterpillars and is highly attracted to Spodoptera exigua-induced plant volatiles. The plasticity of C. marginiventris associative learning to volatile blends of various stimuli, such as host presence, also has been shown, but little is known about how this generalist parasitoid distinguishes between host species of varying suitability. Spodoptera exigua is an excellent host that yields high parasitoid emergence, while Trichoplusia ni serves as a sub-optimal host species due to high pre-imaginal wasp mortality. We have found that S. exigua and T. ni induce different volatile blends while feeding on cotton. Here, wind tunnel flight assays were used to determine the importance of differentially induced volatiles in host-finding by C. marginiventris. We found that, while this generalist parasitoid wasp can distinguish between the two discrete volatile blends when presented concurrently, a positive oviposition experience on the preferred host species (S. exigua) is more important than host-specific volatile cues in eliciting flight behavior towards plants damaged by either host species. Furthermore, wasps with oviposition experience on both host species did not exhibit a deterioration in positive flight behavior, suggesting that oviposition in the sub-optimal host species (T. ni) does not cause aversive odor association.     

Attraction of the Parasitoid <Emphasis Type="Italic">Anagrus nilaparvatae</Emphasis> to Rice Volatiles Induced by the Rice Brown Planthopper <Emphasis Type="Italic">Nilaparvata lugens</Emphasis>

Anagrus nilaparvatae, an egg parasitoid of the rice brown planthopper Nilaparvata lugens, was attracted to volatiles released from N. lugens-infested plants, whereas there was no attraction to volatiles from undamaged plants, artificially damaged plants, or volatiles from N. lugens nymphs, female adults, eggs, honeydew, and exuvia. There was no difference in attractiveness between plants infested by N. lugens nymphs or those infested by gravid females. Attraction was correlated with time after infestation and host density; attraction was only evident between 6 and 24 hr after infestation by 10 adult females per plant, but not before or after. Similarly, after 24 hr of infestation, wasps were attracted to plants with 10 to 20 female planthoppers, but not to plants with lower or higher numbers of female planthoppers. The attractive time periods and densities may be correlated with the survival chances of the wasps' offspring, which do not survive if the plants die before the wasps emerge. Wasps were also attracted to undamaged mature leaves of a rice plant when one of the other mature leaves had been infested by 10 N. lugens for 1 d, implying that the volatile cues involved in host location by the parasitoid are systemically released. Collection and analyses of volatiles revealed that 1 d of N. lugens infestation did not result in the emission of new compounds or an increase in the total amount of volatiles, but rather the proportions among the compounds in the blend were altered. The total amounts and proportions of the chemicals were also affected by infestation duration. These changes in volatile profiles might provide the wasps with specific information on host habitat quality and thus could explain the observed behavioral responses of the parasitoid.     

Effects of Volatiles from Maruca vitrata Larvae and Caterpillar-Infested Flowers of Their Host Plant Vigna unguiculata on the Foraging Behavior of the Parasitoid Apanteles taragamae

The parasitoid wasp Apanteles taragamae is a promising candidate for the biological control of the legume pod borer Maruca vitrata, which recently has been introduced into Benin. The effects of volatiles from cowpea and peabush flowers and Maruca vitrata larvae on host selection behavior of the parasitoid Apanteles taragamae were investigated under laboratory conditions by using a Y-tube olfactometer. Na?ve and oviposition-experienced female wasps were given a choice between several odor sources that included (1) uninfested, (2) Maruca vitrata-infested, and (3) mechanically damaged cowpea flowers, as well as (4) stem portions of peabush plants carrying leaves and flowers, (5) healthy M. vitrata larvae, and moribund (6), and live (7) virus-infected M. vitrata larvae. Responses of na?ve and oviposition-experienced female wasps did not differ for any of the odor source combinations. Wasps were significantly attracted to floral volatiles produced by cowpea flowers that had been infested with M. vitrata larvae and from which the larvae had been removed. Apanteles taragamae females also were attracted to Maruca vitrata-infested flowers after removal of both the larvae and their feces. Female wasps discriminated between volatiles from previously infested flowers and mechanically damaged flowers. Uninfested cowpea flowers attracted only oviposition-experienced wasps that had received a rewarding experience (i.e. the parasitization of two M. vitrata larvae feeding on cowpea flowers) before the olfactometer test. Wasps also were attracted to uninfested leaves and flowers of peabush. Moreover, they were also attracted to healthy and live virus-infected M. vitrata larvae, but not when the latter were moribund. Our data show that, similarly to what has been extensively been reported for foliar volatiles, flowers of plants also emit parasitoid-attracting volatiles in response to being infested with an herbivore.     

Attraction ofCarpophilus Spp. (Coleoptera: Nitidulidae) to volatile compounds present in figs

Various volatile compounds present in ripening figs were attractive toCarpophilus hemipterus, C. mutilatus, C.freemani, andC. lugubris. Field tests demonstrated that traps baited with a mixture of acetaldehyde, ethyl alcohol, and ethyl acetate caught more adultC. hemipterus than those baited with (1) other mixtures involving various combinations of 19 compounds, (2) with 16 single compounds, or (3) with fig paste.This investigation was supported in part by a grant from the California Dried Fig Advisory Board.     

Antennal electrophysiological responses of three parasitic wasps to caterpillar-induced volatiles from maize (Zea mays mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata)

Many parasitic wasps are attracted to volatiles that are released by plants when attacked by potential hosts. The attractiveness of these semiochemicals from damaged plants has been demonstrated in many tritrophic systems, but the physiological mechanisms underlying the insect responses are poorly understood. We recorded the antennal perception by three parasitoids (Cotesia marginiventris, Microplitis rufiventris, and Campoletis sonorensis) to volatiles emitted by maize, cowpea, and cotton plants after attack by the common caterpillar pest Spodoptera littoralis. Gas chromatography-electroantennography (GC-EAG) recordings showed that wasps responded to many, but not all, of the compounds present at the physiologically relevant levels tested. Interestingly, some minor compounds, still unidentified, elicited strong responses from the wasps. These results indicate that wasps are able to detect many odorant compounds released by the plants. It remains to be determined how this information is processed and leads to the specific behavior of the parasitoids.     

Host-recognizing kairomones for parasitic wasp,Anisopteromalus calandrae,from larvae of azuki bean weevil,Callosobruchus chinensis

Host-recognizing kairomones for the stinging behavior of the parasitic wasp, Anisopteromalus calandrae, were identified on host azuki bean weevil larvae, Callosobruchus chinensis (L.). The kairomones were extracted with acetone from Chinese green beans, from which emerged wasps and host weevils had been removed. The kairomones are a mixture of triacylglycerols and fatty acids, each of which is separately active, and with no observable synergistic effect between them. These compounds are known to be constituents of an oviposition-marking pheromone of host azuki bean weevils. However, they differ from the previously reported saturated hydrocarbons and diacylglycerols of the kairomone that another parasitic wasp, Dinarmus basalis, uses for the host recognition of C. chinensis. Thus, A. calandrae and D. basalis selectively utilize different constituents of the oviposition-marking pheromone of C. chinensis as host-recognizing kairomones.     

Parasitic Wasp, Dinarmus basalis, Utilizes Oviposition-marking Pheromone of Host Azuki Bean Weevils As Host-Recognizing Kairomone

A host-recognizing kairomone responsible for the stinging behavior of the parasitic wasp, Dinarmus basalis, was studied. Fresh azuki beans coated with an acetone extract of the azuki beans, from which both emerged wasps and their host weevils were removed, elicited stinging behavior from female wasps. The kairomone is a mixture of saturated hydrocarbons and diacylglycerols, both of which are required for activity. The kairomone is composed of normal and methyl-branched hydrocarbons with carbon numbers ranging from 25 to 35, most of which are known as the hydrocarbon constituents of an oviposition-marking pheromone of the host azuki bean weevils, Callosobruchus chinensis. This indicates that D. basalis utilizes the oviposition-marking pheromone of its host weevils as a host-recognizing kairomone.     

Discriminant analysis of cuticular hydrocarbons of social waspPolistes exclamans viereck and surface hydrocarbons of its nest paper and pedicel

The articular lipids were analyzed from individualPolistes exclamans workers collected from 10 nests. Surface lipids were also recovered from the paper and pedicels of these nests. Twenty-two hydrocarbons were identified in these lipid fractions. The major components of the wasp cuticular lipids weren-heptacosane,n-nonacosane, methylhentriacontane, and methyltritriacontane. Discriminant analysis of the hydrocarbon profiles of the adult wasps showed that the wasps group together according to their respective colonies. Several colonies from the same geographical location clustered more closely together than colonies from diverse locations. The nest papers and pedicels did not group with the wasps from their respective colonies, but the nest papers clustered together separately, as did the nest pedicels.     

Behavioral response ofTrichogramma pretiosum riley andTelenomus sphingis (Ashmead) to trichome/methyl ketone mediated resistance in tomato

Effects of methyl ketone (2-tridecanone and 2-undecanone)/glandular trichome-based resistance to insects ofLycopersicon hirsutum f.glabratum C.H. Mull, PI 134417, on the behavioral responses ofTrichogramma pretiosum Riley andTelenomus sphingis (Ashmead) were observed in the laboratory. ForT. pretiosum, these effects included (1) longer time required by the wasps to cross a leaf disk (diam. 16.3 mm), (2) higher percentage of wasps initiating flight from disks before reaching the edge, and (3) entrapment of wasps in trichome exudates. In tomato genotypes with varying densities of type VI glandular trichomes (3.1–9.2/mm²) but with no methyl ketones in the trichome tips, no such adverse effects were observed. The time taken to cross a disk or initiate flight byT. sphingis, a larger wasp thanT. pretiosum, was not significantly affected on 16.3-mm leaf disks, although the percentage ofT. sphingis initiating flight was directly correlated with trichome density among lines with no ketones. When placed on whole leaflets of plant lines with or without methyl ketones,T. sphingis was entangled by trichome exudates. However, unlikeT. pretiosum, T. sphingis was eventually able to free itself from entanglement. Landing rates byT. sphingis on PI 134417 foliage contained in dialysis tubes were also reduced. Data indicate that suppression of egg parasitism byT. sphingis on resistant foliage is due to both repellent action of its foliar volatiles and reduced searching rates by the parasitoids. Results indicate that a significant portion of the reduction of egg parasitism byT. pretiosum andT. sphingis is attributable to the effects of 2-tridecanone and/or 2-undecanone present in the tips of type VI glandular trichomes on PI 134417 foliage, although the trichomes also adversely affect the wasps even in plant lines without ketones.     

Surface lipids of the social waspPolistes annularis (L.) and its nest and nest pedicel

Cuticular lipids were recovered fromPolistes annularis workers and characterized by combined gas-chromatography-mass spectrometry. These lipids were found to be straight-chain and methyl-branched hydrocarbons with the major components being 13,17-dimethylhentriacontane (18%), 3-methyl-nonacosane (13%), and 3-methylheptacosane (11%). Cuticular lipids with a very similar composition were found on the surface of the larvae, eggs, and adult males ofPolistes annularis as well as on the surface of the nest and nest pedicel of the wasp. Hexadecanoic acid and octadecenoic acid were also found on the surface of the nest pedicel and these acids and/or the hydrocarbons may play a defensive role for the wasps.     

Electrophysiological and Behavioral Evidence for a Sex Pheromone in the Wasp Bephratelloides pomorum

Field experiments showed that males of the seed-feeding, Neotropical wasp Bephratelloides pomorum are strongly attracted to females. That this attraction was semiochemically mediated was demonstrated by both the response of male antennae to the whole-body extract of females and by behavioral bioassays. In the field, males were captured in traps baited with female thoraces, but not with other body parts (abdomen and head). Volatiles collected from the headspace of female wasps or whole-body extracts, concentrated and transferred to cotton plugs, elicited a full sequence of sexual behavior in male wasps. The attraction of males to female-baited traps showed a peak of activity at noon, but in indoor bioassays male responded to female extracts even at night.