Identification of Volatiles That Are Used in Discrimination Between Plants Infested with Prey or Nonprey Herbivores by a Predatory Mite

Carnivorous arthropods can use herbivore-induced plant volatiles to locate their herbivorous prey. In the field, carnivores are confronted with information from plants infested with herbivores that may differ in their suitability as prey. Discrimination by the predatory mite Phytoseiulus persimilis between volatiles from lima bean plants infested with the prey herbivore Tetranychus urticae, or plants infested with the nonprey caterpillar Spodoptera exigua, depends on spider mite density. In this article, we analyzed the chemical composition of the volatile blends from T. urticae-infested lima bean plants at different densities of spider mites, and from S. exigua-infested plants. Based on the behavioral preferences of P. persimilis and the volatile profiles, we selected compounds that potentially enable the mite to discriminate between T. urticae-induced and S. exigua-induced volatiles. Subsequently, we demonstrated in Y-tube olfactometer assays that the relatively large amounts of methyl salicylate and (3E, 7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene emitted by T. urticae-infested bean plants compared to S. exigua-infested plants enable the predators to discriminate. Our data show that specific compounds from complex herbivore-induced volatile blends can play an important role in the selective foraging behavior of natural enemies of herbivorous arthropods.     

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.     

The Response of Phytoseiulus persimilis to Spider Mite-Induced Volatiles from Gerbera: Influence of Starvation and Experience

When leaves of the ornamental crop Gerbera jamesonii are damaged by the spider mite Tetranychus urticae, they produce many volatile compounds in large quantities. Undamaged gerbera leaves produce only a few volatiles in very small quantities. In the headspace of spider mite-damaged gerbera leaves many terpenoids are present, comprising 65% of the volatile blend. In addition, a number of nitrogen containing compounds, such as oximes and nitriles, are produced.We studied the attraction of P. persimilis to the volatiles from spider mite-damaged gerbera leaves and how attraction is affected by starvation and previous experience. Phytoseiulus persimilis that were reared on spider mites (T. urticae) on Lima bean were not attracted to spider mite-induced volatiles from gerbera. Starvation did not influence the predator's response to these volatiles. In contrast, predators that were reared on spider mites on gerbera leaves were strongly attracted to volatiles from spider mite-infested gerbera. This was found also for predators that originated from a culture on spider mite-infested bean and were offered six days of experience with spider mites on gerbera leaves.     

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.     

Behavioral Response of Female Codling Moths, Cydia pomonella, to Apple Volatiles

Apple volatiles stimulated pheromone release, oviposition, and upwind orientation in female codling moths, Cydia pomonella. Green apples increased the percentage of virgin females calling, the duration of female calling, and advanced the onset of egg-laying in gravid females. In a tube olfactometer, both virgin and mated females were more active in the presence of apple volatiles than in clean air. They responded by walking while wing-fanning; mated females showed a stronger attraction response than unmated females.     

Essential Compounds in Herbivore-Induced Plant Volatiles that Attract the Predatory Mite <Emphasis Type="Italic">Neoseiulus womersleyi</Emphasis>

Carnivorous arthropods use volatile infochemicals emitted from prey-infested plants in their foraging behavior. Although several volatile components are common among plant species, the compositions differ among prey–plant complexes. Studies showed that the predatory mite Neoseiulus womersleyi is attracted only to previously experienced plant volatiles. In this study, we identified the attractant components in prey-induced plant volatiles of two prey–plant complexes. N. womersleyi reared on Tetranychus kanzawai-infested tea leaves showed significant preference for a mixture of three synthetic compounds [mimics of the T. kanzawai-induced tea leaves volatiles: (E)-β-ocimene, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), and (E,E)-α-farnesene] at a level comparable to that for T. kanzawai-induced tea plant volatiles. However, mixtures lacking any of these compounds did not attract the predatory mites. Likewise, N. womersleyi reared on T. urticae-infested kidney bean plants showed a significant preference for a mixture of four synthetic compounds [mimics of the T. urticae-induced kidney bean volatiles: DMNT, methyl salicylate (MeSA), β-caryophyllene, and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene] at a level comparable to that for T. urticae-induced kidney bean volatiles. The absence of any of the four compounds resulted in no attraction. These results indicate that N. womersleyi can use at least four volatile components to identify prey-infested plants.     

Electrophysiological and Behavioral Responses of the Cabbage Moth to Plant Volatiles

Plant volatiles from cabbage and chrysanthemum were studied as to how they affect behavior of the cabbage moth, Mamestra brassicae (L.). Chemical, electrophysiological, and behavioral techniques were used. The electroantennographic (EAG) evaluation of selected compounds from Brassi-caceae showed that isothiocyanates (NCS) elicited weak responses, and some did not evoke significant EAG responses at all. Green leaf volatiles (GLVs) evoked the strongest responses in both male and female antennae. The capacity of NCS to stimulate upwind flight of mated females was not different at doses of 10^–7, 10^–6, or 10^–5 g when tested in a wind tunnel. At the higher doses, allyl NCS stimulated upwind flight in the females more than the other compounds. Allyl NCS was significantly better than the other compounds at stimulating females to land on targets. Mated females flew upwind and landed on the targets with allyl NCS more often than virgin females and males. With respect to the behavioral activity of GLVs, only (E)-2-hexenal and (Z)-3-hexenyl acetate elicited upwind flight and landing in females. Ten compounds were identified from a chrysanthemum extract by using coupled gas chromatography–electroantennography. Five of these, (Z)-3-hexenyl acetate, 1-8-cineole, -terpinene, chrysanthenone, and camphor, elicited upwind flight of mated females, but only three stimulated landing.     

Herbivore-induced Plant Volatiles Trigger Sporulation in Entomopathogenic Fungi: The Case of <Emphasis Type="Italic">Neozygites tanajoae</Emphasis> Infecting the Cassava Green Mite

A large body of evidence shows that plants release volatile chemicals upon attack by herbivores. These volatiles influence the performance of natural enemies. Nearly all the evidence on the effect of plant volatiles on natural enemies of herbivores concerns predators, parasitoids, and entomophagous nematodes. However, other entomopathogens, such as fungi, have not been studied yet for the way they exploit the chemical information that the plant conveys on the presence of herbivores. We tested the hypothesis that volatiles emanating from cassava plants infested by green mites (Mononychellus tanajoa) trigger sporulation in three isolates of the acaropathogenic fungus Neozygites tanajoae. Tests were conducted under climatic conditions optimal to fungal conidiation, such that the influence of the plant volatiles could only alter the quantity of conidia produced. For two isolates (Altal.brz and Colal.brz), it was found that, compared with clean air, the presence of volatiles from clean, excised leaf discs suppressed conidia production. This suppressive effect disappeared in the presence of herbivore-damaged leaves for the isolate Colal.brz. For the third isolate, no significant effects were observed. Another experiment differing mainly in the amount of volatiles showed that two isolates produced more conidia when exposed to herbivore-damaged leaves compared with clean air. Taken together, the results show that volatiles from clean plants suppress conidiation, whereas herbivore-induced plant volatiles promote conidiation of N. tanajoae. These opposing effects suggest that the entomopathogenic fungus tunes the release of spores to herbivore-induced plant signals indicating the presence of hosts.     

Host Plant Volatiles Synergize Response to Sex Pheromone in Codling Moth, Cydia pomonella

Plant volatile compounds synergize attraction of codling moth males Cydia pomonella to sex pheromone (E,E)-8,10-dodecadien-1-ol (codlemone). Several apple volatiles, known to elicit a strong antennal response, were tested in a wind tunnel. Two-component blends of 1 pg/min codlemone and 100 pg/min of either racemic linalool, (E)-beta-farnesene, or (Z)-3-hexen-1-ol attracted significantly more males to the source than codlemone alone (60, 58, 56, and 37%, respectively). In comparison, a blend of codlemone and a known pheromone synergist, dodecanol, attracted 56% of the males tested. Blends of pheromone and plant volatiles in a 1:100 ratio attracted more males than 1:1 or 1:10,000 blends. Adding two or four of the most active plant compounds to codlemone did not enhance attraction over blends of codlemone plus single-plant compounds. Of the test compounds, only farnesol was attractive by itself; at a release rate of 10,000 pg/min, 16% of the males arrived at the source. However, attraction to a 1:10,000 blend of codlemone and farnesol (42%) was not significantly different from attraction to codlemone alone (37%). In contrast, a codlemone mimic, (E)-10-dodecadien-1-ol, which attracted 2% males by itself, had a strong antagonistic effect when blended in a 1:10,000 ratio with codlemone.     

Foraging Behavior of Anastrepha Ludens, A. obliqua, and A. serpentina in Response to Feces Extracts Containing Host Marking Pheromone

Following oviposition, females of many Tephritid flies deposit host marking pheromones (HMPs) to indicate that the host fruit has been occupied. We describe the foraging behavior of these three economically important species (Anastrepha ludens and A. obliqua from the fraterculus species group and A. serpentina from the serpentina species group) when they encounter an artificial fruit (green agar spheres wrapped in Parafilm) marked with intra- and interspecific feces extracts that contain, among other substances, host marking pheromone. When flies encountered fruit treated with either 1 or 100 mg/ml feces extract, there were drastic and statistically significant reductions in tree residence time, mean time spent on fruit, and in the number of oviposition attempts or actual ovipositions when compared to the control treatment (clean fruit). These responses were almost identical irrespective of extract origin (i.e., fly species), indicating complete interspecific HMP cross-recognition by all three Anastrepha species tested. We discuss the ecological and practical implications of our findings.     

Orientation of boll weevil,Anthonomus grandis boh. (Coleoptera: Curculionidae), to pheromone and volatile host compound in the laboratory

Behavioral responses of male and female boll weevils to the aggregation pheromone, grandlure, and the major volatile of cotton, -bisabolol, were investigated using a new dual-choice olfactometer. Dosage-response experiments revealed both males and females to be attracted by the aggregation pheromone at the 1.0 g dosage. However, only males were attracted to -bisabolol (1.0 g). Both sexes were repelled by the highest dosage of-bisabolol tested (10 g). In preference experiment, males chose grandlure over -bisabolol, while both sexes chose the combination of grandlure + -bisabolol over -bisabolol alone. There was some evidence for synergism between pheromone and plant odor for the females. The results correlate well with previous electrophysiological and behavioral experiments.Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products or vendors that may also be suitable.     

Function of Aggregation Pheromone in the Larger Grain Borer Prostephanus truncatus: Variation in Response to Individuals as Evidence for a Role in Sexual Selection

The ability of both male and female Prostephanus truncatus beetles to distinguish between the aggregation pheromone signals of two closely located conspecific male beetles was investigated by using an olfactometer. Beetles detected variation between male signalers and visited some signalers more than others. Beetles of both sexes were found to make the same choices. These patterns of preference were found to be mirrored in trap catches of dispersing beetles when single males were used to bait flight traps that were placed in pairs in a woodland habitat in Ghana. The results are discussed with reference to the hypothesis that males signal primarily to attract mates and, therefore, features of the aggregation-pheromone signal may be sexually selected. The implications of the results for current and possible future pest-management tools are also explored.     

Shifts in Life-History Traits as a Response to Cannibalism in Larval Long-Toed Salamanders (Ambystoma macrodactylum)

We examined the potential influence of cannibalism on life-history characteristics of larval long-toed salamanders (Ambystoma macrodactylum). Using a 2 × 2 factorial design, crossing morphology with diet, we exposed typical morph larvae to one of four types of stimulus animals: cannibal morphs fed a conspecific diet, cannibal morphs fed a heterospecific diet (i.e., Tubifex), typical morphs fed a conspecific diet, and typical morphs fed a heterospecific diet. Test larvae exposed to stimulus animals fed a conspecific diet exhibited a slower growth rate and an increase in the time taken to reach metamorphosis. These changes in life history likely represent a cost of antipredator behavior.     

Predatory Behavior of <Emphasis Type="Italic">Polistes dominulus</Emphasis> Wasps in Response to Cardenolides and Glucosinolates in <Emphasis Type="Italic">Pieris napi</Emphasis> Caterpillars

To examine how plant allelochemicals in prey affect foraging choices made by generalist predator paper wasps, Polistes dominulus (Vespidae), we compared predation on Pieris napi (Pieridae) caterpillars reared on host plants with different allelochemicals. In naturalistic behavioral choice experiments, free-flying wasps chose between living pierids reared on cabbage (Brassica oleracea), which lacks deterrent allelochemicals, or alternate host plants with potentially deterrent allelochemicals. The alternative host plants were: wormwood mustard, (Erysimum cheiranthoides: Brassicaceae), which contains cardenolides; nasturtium (Tropaeolum majus: Tropaeolaceae) with high concentrations of chlorogenic acid; and black mustard (Brassica nigra: Brassicaceae) with high concentrations of the aliphatic glucosinolate, sinigrin. Although wasps captured equal numbers of caterpillars reared on cabbage and each alternate host plant, they spent significantly longer handling prey from the alternate host plants as they selectively removed the caterpillar’s gut, which contained the plant material. This was true even if the caterpillar did not sequester toxins in its tissues, as revealed by high performance liquid chromatography (HPLC) analysis of Erysimum-reared pierids. Because handling time is longer, predators that capture pierids containing non-sequestered allelochemicals experience an overall reduction in foraging rate that may translate into a fitness cost.