Volatile Stimuli Related to Feeding Activity of Nonprey Caterpillars, Spodoptera exigua, Affect Olfactory Response of the Predatory Mite Phytoseiulus persimilis

The effect of volatiles related to feeding activity of nonprey caterpillars, Spodoptera exigua, on the olfactory response of the predatory mites Phytoseiulus persimilis was examined in a Y-tube olfactometer. At a low caterpillar density (20 caterpillars on 10 Lima bean leaves), the predators were significantly more attracted to volatiles from infested leaves on which the caterpillars and their products were present or from infested leaves from which the caterpillars and their products had been removed when compared to volatiles from uninfested leaves. The predators, however, significantly avoided odors from 20 caterpillars and their products (mainly feces) removed from bean leaves. In contrast, at a higher caterpillar density (100 caterpillars on 10 Lima bean leaves), the predators avoided volatiles from caterpillar-infested bean leaves. Volatiles from infested leaves from which the caterpillars and their products had been removed were not preferred over volatiles from uninfested leaves. Volatiles from feces collected from 100 caterpillars were strongly avoided by the predators, while the behavior of the predatory mites was not affected by volatiles from 100 caterpillars removed from a plant. The data show that carnivorous arthropods may avoid nonprofitable herbivores. This avoidance seems to result from an interference of volatiles from herbivore products with the attraction to herbivore-induced plant volatiles.     

Induction of Direct and Indirect Plant Responses by Jasmonic Acid, Low Spider Mite Densities, or a Combination of Jasmonic Acid Treatment and Spider Mite Infestation

Jasmonic acid (JA) and the octadecanoid pathway are involved in both induced direct and induced indirect plant responses. In this study, the herbivorous mite, Tetranychus urticae, and its predator, Phytoseiulus persimilis, were given a choice between Lima bean plants induced by JA or spider mites and uninduced control plants. Infestation densities resulting in the induction of predator attractants were much lower than thus far assumed, i.e., predatory mites were significantly attracted to plants that were infested for 2 days with only one or four spider mites per plant. Phytoseiulus persimilis showed a density-dependent response to volatiles from plants that were infested with different numbers of spider mites. Similarly, treating plants with increasing concentrations of JA also led to increased attraction of P. persimilis. Moreover, the duration of spider mite infestation was positively correlated with the proportion of predators that were attracted to mite-infested plants. A pretreatment of the plants with JA followed by a spider mite infestation enhanced the attraction of P. persimilis to plant volatiles compared to attraction to volatiles from plants that were only infested with spider mites and did not receive a pretreatment with JA. The herbivore, T. urticae preferred leaf tissue that previously had been infested with conspecifics to uninfested leaf tissue. In the case of choice tests with JA-induced and control leaf tissue, spider mites slightly preferred control leaf tissue. When spider mites were given a choice between leaf discs induced by JA and leaf discs damaged by spider mite feeding, they preferred the latter. The presence of herbivore induced chemicals and/or spider mite products enhanced settlement of the mites, whereas treatment with JA seemed to impede settlement.     

Change in Behavioral Response to Herbivore-induced Plant Volatiles in a Predatory Mite Population

Damage by herbivorous spider mites induces plants to produce volatiles that attract predatory mites that consume the spider mites. A clear attraction to volatiles from Lima bean plants infested with the spider mite Tetranychus urticae has been consistently reported during more than 15 years for the predatory mite Phytoseiulus persimilis. We have monitored the response to volatiles from spider-mite infested Lima bean plants for a laboratory population of the predatory mite from 1991 to 1995 on a regular basis. A reduction in the level of attraction in the laboratory population of P. persimilis was recorded in mid-1992. The attraction of the laboratory population was weaker than that of a commercial population in the latter part of 1992, but the responses of these two populations were similarly weak in 1994 and 1995. Therefore, a behavioral change has also occurred in this commercial population. Experiments were carried out to address the potential causes of this change in attraction. The attraction of predators from a commercial population with a strong response decreased after being reared in our laboratory. Within a predator population with a low degree of attraction, strongly responding predators were present and they could be isolated on the basis of their behavior: predators that stayed on spider-mite infested plants in the rearing set-up had a strong attraction, while predators that had dispersed from the rearing set-up were not attracted to prey-infested bean plants. From our laboratory population with a low degree of attraction, isofemale lines were initiated and maintained for more than 20 generations. All isofemale lines exhibited a consistently strong attraction to spider mite-induced plant volatiles, similar to the attraction recorded for several populations in the past 15 years. Neither in a population with a strong attraction nor in two with a weak attraction was the response of the predators affected by a starvation period of 1–3 hr. Based on these results, possible causes for the observed reduction in predator attraction to spider mite-induced bean volatiles are discussed. The predatory mite P. persimilis is a cornerstone of biological control in many crops worldwide. Therefore, the change in foraging behavior recorded in this predator may have serious consequences for biological control of spider mites.     

Olfactory Responses of Banana Weevil Predators to Volatiles from Banana Pseudostem Tissue and Synthetic Pheromone

As a response to attack by herbivores, plants can emit a variety of volatile substances that attract natural enemies of these insect pests. Predators of the banana weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) such as Dactylosternum abdominale (Coleoptera: Hydrophilidae) and Pheidole megacephala (Hymenoptera: Formicidae), are normally found in association with weevil-infested rotten pseudostems and harvested stumps. We investigated whether these predators are attracted to such environments in response to volatiles produced by the host plant, by the weevil, or by the weevil–plant complex. We evaluated predator responses towards volatiles from banana pseudostem tissue (synomones) and the synthetic banana weevil aggregation pheromone Cosmolure+ in a two-choice olfactometer. The beetle D. abdominale was attracted to fermenting banana pseudostem tissue and Cosmolure+, whereas the ant P. megacephala was attracted only to fermented pseudostem tissue. Both predators were attracted to banana pseudostem tissue that had been damaged by weevil larvae irrespective of weevil presence. Adding pheromone did not enhance predator response to volatiles from pseudostem tissue fed on by weevils. The numbers of both predators recovered with pseudostem traps in the field from banana mats with a pheromone trap were similar to those in pseudostem traps at different distance ranges from the pheromone. Our study shows that the generalist predators D. abdominale and P. megacephala use volatiles from fermented banana pseudostem tissue as the major chemical cue when searching for prey.     

The Involvement of Volatile Infochemicals from Spider Mites and from Food-Plants in Prey Location of the Generalist Predatory Mite <Emphasis Type="Italic">Neoseiulus californicus</Emphasis>

We investigated volatile infochemicals possibly involved in location of the generalist predatory mite Neoseiulus californicus to plants infested with spider mites in a Y-tube olfactometer. The predators significantly preferred volatiles from lima bean leaves infested with Tetranychus urticae to uninfested lima bean leaves. Likewise, they were attracted to volatiles from artificially damaged lima bean leaves and those from T. urticae plus their visible products. Significantly more predators chose infested lima bean leaves from which T. urticae plus their visible products had been removed than artificially damaged leaves, T. urticae, and their visible products. These results suggest that N. californicus is capable of exploiting a variety of volatile infochemicals originating from their prey, from the prey-foodplants themselves, and from the complex of the prey and the host plants (e.g., herbivore-induced volatiles). We also investigated predator response to some of the synthetic samples identified as volatile components emitted from T. urticae-infested lima bean leaves and/or artificially damaged lima bean leaves. The predators were attracted to each of the five synthetic volatile components: linalool, methyl salicylate, (Z)-3-hexen-1-ol, (E)-2-hexenal, and (Z)-3-hexenyl acetate. The role of each volatile compound in prey-searching behavior is discussed.     

Influence of Synthetic Oviposition Pheromone and Volatiles from Soakage Pits and Grass Infusions Upon Oviposition Site-Selection of Culex Mosquitoes in Tanzania

The response of Culex mosquitoes to (5R,6S)-6-acetoxy-5-hexadecanolide (the synthetic oviposition pheromone, SOP), emanations from soakage pit water (SPW), and grass infusions (GI) was studied in pit latrines in Muheza, Tanzania. Water treated with the synthetic oviposition pheromone received more egg rafts of Culex quinquefasciatus Say and Cx. cinereus Theobald than did the untreated water (P < 0.001). The residual activity of SOP did not decrease over a nine-day period, with the geometric mean number of egg rafts laid in the SOP-treated water varying daily between 2.5 and 8.9 as compared to 0.1–1.6 egg rafts laid in tap water. However, SOP did not attract ovipositing mosquitoes to nonbreeding sites, and both treatment and control received few eggs. SPW and GI attracted ovipositing Cx. quinquefasciatus, Cx. cinereus, and Cx. tigripes Grandpré and de Charmoy with the number of eggs rafts deposited in bowls containing SPW or GI being larger than that deposited in bowls with tap water (P < 0.05). More egg rafts of Cx. quinquefasciatus were deposited in SOP-treated water than in SPW (P < 0.05). When SOP was compared with SOP + SPW, more egg rafts of Cx. quinquefasciatus were deposited in bowls with the latter combination than in bowls containing SOP or SPW only (P < 0.05), indicating a synergistic effect between SOP and SPW. Similarly, when SOP-treated water and GI were compared with SOP + GI, more egg rafts of Cx. quinquefasciatus were laid in the latter bowl, indicating a synergistic effect between SOP and GI. The result suggest that the combined use of SOP and organically enriched water can be employed in monitoring of Cx. quinquefasciatus for control programs. This is the first record of the attraction of Cx. cinereus and Cx. tigripes to oviposition stimuli.     

Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: Extraction of endogenous elicitor

It was previously shown that in response to infestation by spider mites (Tetranychus urticae), lima bean plants produce a volatile herbivoreinduced synomone that attracts phytoseiid mites (Phytoseiulus persimilis) that are predators of the spider mites. The production of predator-attracting infochemicals was established to occur systemically throughout the spider mitein-fested plant. Here we describe the extraction of a water-soluble endogenous elicitor from spider mite-infested lima bean leaves. This elicitor was shown to be transported out of infested leaves and was collected in water in which the petiole of the infested leaf was placed. When the petioles of uninfested lima bean leaves were placed in water in which infested leaves had been present for the previous seven days, these uninfested lima bean leaves became highly attractive to predatory mites in an olfactometer when an appropriate control of uninfested lima bean leaves was offered as alternative. The strength of this effect was dependent on the number of spider mites infesting the elicitor-producing leaves. Higher numbers of spider mites resulted in an elicitor solution with a stronger effect. In addition, spider mite density was important. The elicitor obtained from one leaf with 50 spider mites had a stronger effect on the attractiveness of uninfested leaves than the elicitor obtained from three leaves with 17 spider mites each. This suggests that the stress intensity imposed on a plant is an important determinant of the elicitor quantity. While the elicitor has a strong effect on the attractiveness of uninfested leaves, spider mite-infested leaves are still much more attractive to predatory mites than elicitor-exposed leaves. The data are discussed in the context of systemic effects in plant defense and the biosynthesis of herbivore-induced terpenoids in plants.     

Response of the Pollen Beetle, Meligethes aeneus, to Traps Baited with Volatiles from Oilseed Rape, Brassica napus

The response of the pollen beetle, Meligethes aeneus, to yellow water traps baited with individual lures of 25 floral volatile compounds was studied in 17 field experiments. The compounds comprised seven nitrogenous amino acid derivatives, five nonnitrogenous amino acid derivatives, nine fatty acid derivatives, and four isoprenoids. Twenty compounds affected the trap catch of M. aeneus, but response was often dependent on release rate. Most compounds were attractive, but four fatty acid derivatives were repellent. 1-Hexanol was either attractive or repellent, depending on the release rate. It is suggested that M. aeneus responds to this large number of chemically diverse compounds because it is polyphagous.     

The Role of Fresh <Emphasis Type="Italic">versus</Emphasis> Old Leaf Damage in the Attraction of Parasitic Wasps to Herbivore-Induced Maize Volatiles

The odor produced by a plant under herbivore attack is often used by parasitic wasps to locate hosts. Any type of surface damage commonly causes plant leaves to release so-called green leaf volatiles, whereas blends of inducible compounds are more specific for herbivore attack and can vary considerably among plant genotypes. We compared the responses of naïve and experienced parasitoids of the species Cotesia marginiventris and Microplitis rufiventris to volatiles from maize leaves with fresh damage (mainly green leaf volatiles) vs. old damage (mainly terpenoids) in a six-arm olfactometer. These braconid wasps are both solitary endoparasitoids of lepidopteran larvae, but differ in geographical origin and host range. In choice experiments with odor blends from maize plants with fresh damage vs. blends from plants with old damage, inexperienced C. marginiventris showed a preference for the volatiles from freshly damaged leaves. No such preference was observed for inexperienced M. rufiventris. After an oviposition experience in hosts feeding on maize plants, C. marginiventris females were more attracted by a mixture of volatiles from fresh and old damage. Apparently, C. marginiventris has an innate preference for the odor of freshly damaged leaves, and this preference shifts in favor of a blend containing a mixture of green leaf volatiles plus terpenoids, after experiencing the latter blend in association with hosts. M. rufiventris responded poorly after experience and preferred fresh damage odors. Possibly, after associative learning, this species uses cues that are more directly related with the host presence, such as volatiles from host feces, which were not present in the odor sources offered in the olfactometer. The results demonstrate the complexity of the use of plant volatiles by parasitoids and show that different parasitoid species have evolved different strategies to exploit these signals.     

Impact of Botanical Pesticides Derived from Melia azedarach and Azadirachta indica Plants on the Emission of Volatiles that Attract Parasitoids of the Diamondback Moth to Cabbage Plants

Herbivorous and carnivorous arthropods use chemical information from plants during foraging. Aqueous leaf extracts from the syringa tree Melia azedarach and commercial formulations from the neem tree Azadirachta indica, Neemix 4.5^®, were investigated for their impact on the flight response of two parasitoids, Cotesia plutellae and Diadromus collaris. Cotesia plutellae was attracted only to Plutella xylostella-infested cabbage plants in a wind tunnel after an oviposition experience. Female C. plutellae did not distinguish between P. xylostella-infested cabbage plants treated with neem and control P. xylostella-infested plants. However, females preferred infested cabbage plants that had been treated with syringa extract to control infested plants. Syringa extract on filter paper did not attract C. plutellae. This suggests that an interaction between the plant and the syringa extract enhances parasitoid attraction. Diadromus collaris was not attracted to cabbage plants in a wind tunnel and did not distinguish between caterpillar-damaged and undamaged cabbage plants. Headspace analysis revealed 49 compounds in both control cabbage plants and cabbage plants that had been treated with the syringa extract. Among these are alcohols, aldehydes, ketones, esters, terpenoids, sulfides, and an isothiocyanate. Cabbage plants that had been treated with the syringa extract emitted larger quantities of volatiles, and these increased quantities were not derived from the syringa extract. Therefore, the syringa extract seemed to induce the emission of cabbage volatiles. To our knowledge, this is the first example of a plant extract inducing the emission of plant volatiles in another plant. This interesting phenomenon likely explains the preference of C. plutellae parasitoids for cabbage plants that have been treated with syringa extracts.     

Attraction of Female Oriental Fruit Fly, Bactrocera dorsalis, to Volatile Semiochemicals from Leaves and Extracts of a Nonhost Plant, Panax (Polyscias guilfoylei) in Laboratory and Olfactometer Assays

Fresh whole leaves and solvent–water leaf extracts of the hedgerow plant panax, Polyscias guilfoylei (Bull), were tested for their attractiveness to male and female Oriental fruit flies, Bactrocera dorsalis, in laboratory flight tunnel and cage olfactometer bioassays. Fresh mature whole panax leaves were found to be attractive to mated female oriental fruit flies in the flight tunnel. Response of males and virgin females was low and in most instances not significantly different from controls. Attraction of mated female flies to the layers resulting from a methylene chloride–water partition or a hexane–water partition of freshly ground leaves using small McPhail traps was greatest in the methylene chloride fraction. When methylene chloride and water layers were tested competitively in a multiple-choice rotating olfactometer, the methylene chloride fraction was more attractive. Tests involving the methylene chloride–water interface (an emulsion of the two partitioned layers) with and without a standard attractant NuLure, showed the emulsion layer to be significantly more attractive than the other fractions or NuLure. In outdoor cage olfactometer assays of methylene chloride and water fractions, activity was greatest in the methylene chloride fraction. The results suggests that volatile semiochemicals from this nonhost plant are attractive to mated female Oriental fruit flies. The results are discussed in relation to the chemical ecology of B. dorsalis and the potential use of this nonhost plant for detection and control of female Oriental fruit flies in the field.     

Response of the Aphid Parasitoid <Emphasis Type="Italic">Aphidius funebris</Emphasis> to Volatiles from Undamaged and Aphid-infested <Emphasis Type="Italic">Centaurea nigra</Emphasis>

Two issues have hindered the understanding of the ecology and evolution of volatile-mediated tritrophic interactions: few studies have addressed noncrop systems; and few statistical techniques have been applied that are suitable for the analysis of complex volatile blends. In this paper, we addressed both of these issues by studying the noncrop system involving the plant Centaurea nigra, the specialist aphid Uroleucon jaceae, and the parasitoid Aphidius funebris. In a Y-tube olfactometer, A. funebris was attracted to the odor from undamaged C. nigra, but preferred the plant–host complex (PHC) after 3 d of feeding by 200 U. jaceae over the undamaged plant, but not after three or 5 d of feeding by 50 U. jaceae. When aphids were removed, the initial preference for the damaged plant remained, but the final preference was not greater than for the undamaged plant. No qualitative differences were detected between the headspaces of C. nigra and the C. nigra–U. jaceae PHC. For quantitative analysis, we used a compositional approach, which treats each compound produced as part of a blend, and not as a compound released in isolation, thus allowing analysis of the relative contribution of each compound to the blend as a whole. With this approach, subtle increases and decreases of some green leaf volatiles and monoterpenoids on the third day of aphid infestation were detected. Mechanically damaged C. nigra had a volatile profile that differed from undamaged C. nigra and the PHC. One and 10 ng of (Z)-3-hexenyl acetate, and 10 or 100 ng of 6-methyl-5-hepten-2-one were attractive to the parasitoid when placed in solution on filter paper. A. funebris appears to be using a combination of chemical cues to locate host-infested plants.