Induction of Plant Volatiles by Herbivores with Different Feeding Habits and the Effects of Induced Defenses on Host-Plant Selection by Thrips

Induced plant responses to attack by chewing insects have been intensively studied, but little is known about plant responses to nonchewing insects or to attack by multiple herbivores with different feeding habits. We examined volatile emissions by tobacco, Nicotiana tabacum, in response to feeding by the piercing–sucking insect western flower thrips (WFT), Frankliniella occidentalis, the chewing herbivore Heliothis virescens, and both herbivores simultaneously. In addition, we examined the effects of herbivore-induced plant defenses on host-plant selection by WFT. Plants responded to thrips feeding by consistently releasing five compounds. Simultaneous feeding by WFT and H. virescens elicited the same 11 compounds emitted in response to caterpillar feeding alone; however, two compounds, α-humulene and caryophyllene oxide, were produced in greater amounts in response to simultaneous herbivory. In choice tests, thrips consistently preferred uninduced plants over all other treatments and preferred plants damaged by caterpillars and those treated with caterpillar saliva over those treated with caterpillar regurgitant. The results are consistent with a previous finding that caterpillar regurgitant induces the release of significantly more volatile nicotine than plants damaged by caterpillars or plants treated with caterpillar saliva. A repellent effect of nicotine on WFT was confirmed by encircling unwounded plants with septa releasing volatile nicotine. Our results provide the first direct evidence that thrips feeding induces volatile responses and indicates that simultaneous herbivory by insects with different feeding habits can alter volatile emissions. In addition, the findings demonstrate that induced plant responses influence host-plant selection by WFT and suggest that the induction of volatile nicotine may play a role in this process.     

Do Caterpillars Secrete “Oral Secretions”?

The oral secretions or regurgitant of caterpillars contain potent elicitors of plant induced responses. These elicitors are recognized by host plants to differentiate between simple mechanical injury and the presence of herbivores. In some cases, this level of recognition is highly specific. Despite the in-depth chemical characterization of these elicitors, little is known about the amounts delivered in regurgitant during feeding. In this study, we use a fluorescent dye to label regurgitant in order to visualize caterpillar regurgitation during feeding. The procedure is highly sensitive and allows us to visualize nanoliter amounts of regurgitant. We examined the propensity of larval Helicoverpa zea, Heliothis virescens, Spodoptera exigua, Spodoptera frugiperda, and Manduca sexta to regurgitate on various host plants. These species were selected because they have been among the most intensely studied in terms of elicitors. Our results indicate that most larvae did not regurgitate following a brief feeding bout (∼10 min) during which they ate ca. 0.40 cm² of leaf. When larvae did regurgitate, it was typically less than 10 nl. This is several orders of magnitude less than is typically used in most studies on oral secretions. The frequency of regurgitation appears to vary depending upon the host plant. Larval H. zea are less likely to regurgitate when feeding on tomato leaves compared to corn mid-whorl tissue. Our results have importance in understanding the role of oral secretions in plant recognition of herbivory. Because caterpillars did not routinely regurgitate during feeding, it is likely that they avoid the elicitation of some plant defensive responses during most feeding bouts.     

Feeding Experience Affects the Behavioral Response of Polyphagous Gypsy Moth Caterpillars to Herbivore-induced Poplar Volatiles

Plant volatiles influence host selection of herbivorous insects. Since volatiles often vary in space and time, herbivores (especially polyphagous ones) may be able to use these compounds as cues to track variation in host plant quality based on their innate abilities and previous experience. We investigated the behavioral response of naïve (fed on artificial diet) and experienced (fed on poplar) gypsy moth (Lymantria dispar) caterpillars, a polyphagous species, towards constitutive and herbivore-induced black poplar (Populus nigra) volatiles at different stages of herbivore attack. In Y-tube olfactometer assays, both naïve and experienced caterpillars were attracted to constitutive volatiles and volatiles released after short-term herbivory (up to 6 hr). Naïve caterpillars also were attracted to volatiles released after longer-term herbivory (24–30 hr), but experienced caterpillars preferred the odor of undamaged foliage. A multivariate statistical analysis comparing the volatile emission of undamaged plants vs. plants after short and longer-term herbivory, suggested various compounds as being responsible for distinguishing between the odors of these plants. Ten compounds were selected for individual testing of caterpillar behavioral responses in a four-arm olfactometer. Naïve caterpillars spent more time in arms containing (Z)-3-hexenol and (Z)-3-hexenyl acetate than in solvent permeated arms, while avoiding benzyl cyanide and salicyl aldehyde. Experienced caterpillars avoided benzyl cyanide and preferred (Z)-3-hexenyl acetate and the homoterpene (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) over solvent. Only responses to DMNT were significantly different when comparing experienced and naïve caterpillars. The results show that gypsy moth caterpillars display an innate behavioral response towards constitutive and herbivore-induced plant volatiles, but also that larval behavior is plastic and can be modulated by previous feeding experience.     

Transgenic upregulation of the condensed tannin pathway in poplar leads to a dramatic shift in leaf palatability for two tree-feeding Lepidoptera

Transgenic hybrid aspen (Populus tremula x tremuloides) overexpressing the MYB134 tannin regulatory gene show dramatically enhanced condensed tannin (proanthocyanidin) levels, as well as shifts in other phenolic metabolites. A series of insect bioassays with forest tent caterpillars (Malacosoma disstria) and gypsy moth (Lymantria dispar) caterpillars was carried out to determine how this metabolic shift affects food preference and performance of generalist tree-feeding lepidopterans. Both species showed a distinct preference for the high-tannin MYB134 overexpressor plants, and L. dispar performance was enhanced relative to controls. L. dispar reached greater pupal weight and showed reduced time to pupation when reared on the MYB134 overexpressing poplar. These results were unexpected since enhanced condensed tannin levels were predicted to act as feeding deterrents. However, the data may be explained by the observed decrease in the salicinoids (phenolic glycosides) salicortin and tremulacin that accompanied the upregulation of the condensed tannins in the transgenics. We conclude that for these two lepidopteran species, condensed tannin levels are unlikely to be a major determinant of caterpillar food preference or performance. However, our experiments show that overexpression of a single regulatory gene in transgenic aspen can have a significant impact on herbivorous insects.     

Orientation ofMicroplitis croceipes (Hymenoptera: Braconidae) to green leaf volatiles: Dose-response curves

FemaleMicroplitis croceipes wasps were tested in a wind tunnel for their ability to orient to various concentrations of eight different green leaf volatile (GLV) substances [hexanal, (E)-2-hexenal, (E)-2-hexen-1-ol, (Z)-3-hexen-1-ol, (E)-2-hexenyl acetate, (Z)-3-hexenyl acetate, (Z)-3-hexenyl propionate, and (Z)-3-hexenyl butyrate]. Overall, the esters elicited the greatest percentage of successful orientation flights, the alcohols elicited an intermediate response, and the aldehydes elicited a low response. The semilog dose-response curves were generally hill-shaped with high responses at medium release rates and low responses at high or low release rates. For the aldehydes, positive responses occurred at all GLV release rates between 0.01 and 100 nl/min. For some alcohols and esters, positive responses occurred at release rates as low as 1 pl/min and as high as 1μl/min. These data show thatM. croceipes wasps are strongly attracted to GLVs and are capable of orienting to GLV concentrations that would occur in nature when a caterpillar feeds on a green leaf. Hence, in nature, GLVs may be important clues, enablingM. croceipes to locate their hosts.     

Induction of parasitoid attracting synomone in brussels sprouts plants by feeding ofPieris brassicae larvae: Role of mechanical damage and herbivore elicitor

Induction of plant defense in response to herbivory includes the emission of synomones that attract the natural enemies of herbivores. We investigated whether mechanical damage to Brussels sprouts leaves (Brassica oleracea var.gemmifera) is sufficient to obtain attraction of the parasitoidCotesia glomerata or whether feeding byPieris brassicae caterpillars elicits the release of synomones not produced by mechanically damaged leaves. The response of the parasitoidCotesia glomerata to different types of simulated herbivory was observed. Flight-chamber dual-choice tests showed that mechanically damaged cabbage leaves were less attractive than herbivore-damaged leaves and mechanically damaged leaves treated with larval regurgitant. Chemical analysis of the headspace of undamaged, artificially damaged, caterpillar-infested, and caterpillar regurgitant-treated leaves showed that the plant responds to damage with an increased release of volatiles. Greenleaf volatiles and several terpenoids are the major components of cabbage leaf headspace. Terpenoids are emitted in analogous amounts in all treatments, including undamaged leaves. On the other hand, if the plant is infested by caterpillars or if caterpillar regurgitant is applied to damaged leaves, the emission of green-leaf volatiles is highly enhanced. Our data are in contrast with the induction of more specific synomones in other plant species, such as Lima bean and corn.     

Molecular,Biochemical, and Organismal Analyses of Tomato Plants Simultaneously Attacked by Herbivores from Two Feeding Guilds

Previous work identified aphids and caterpillars as having distinct effects on plant responses to herbivory. We sought to decipher these interactions across different levels of biological organization, i.e., molecular, biochemical, and organismal, with tomato plants either damaged by one 3rd-instar beet armyworm caterpillar (Spodoptera exigua), damaged by 40 adult potato aphids (Macrosiphum euphorbiae), simultaneous damaged by both herbivores, or left undamaged (controls). After placing insects on plants, plants were transferred to a growth chamber for 5 d to induce a systemic response. Subsequently, individual leaflets from non-damaged parts of plants were excised and used for gene expression analysis (microarrays and quantitative real-time PCR), C/N analysis, total protein analysis, proteinase inhibitor (PI) analysis, and for performance assays. At the molecular level, caterpillars up-regulated 56 and down-regulated 29 genes systemically, while aphids up-regulated 93 and down-regulated 146 genes, compared to controls. Although aphids induced more genes than caterpillars, the magnitude of caterpillar-induced gene accumulation, particularly for those associated with plant defenses, was often greater. In dual-damaged plants, aphids suppressed 27% of the genes regulated by caterpillars, while caterpillars suppressed 66% of the genes regulated by aphids. At the biochemical level, caterpillars induced three-fold higher PI activity compared to controls, while aphids had no effects on PIs either alone or when paired with caterpillars. Aphid feeding alone reduced the foliar C/N ratio, but not when caterpillars also fed on the plants. Aphid and caterpillar feeding alone had no effect on the amount of protein in systemic leaves; however, both herbivores feeding on the plant reduced the amount of protein compared to aphid-damaged plants. At the organismal level, S. exigua neonate performance was negatively affected by prior caterpillar feeding, regardless of whether aphids were present or absent. This study highlights areas of concordance and disjunction between molecular, biochemical, and organismal measures of induced plant resistance when plants are attacked by multiple herbivores. In general, our data produced consistent results when considering each herbivore separately but not when considering them together.     

Fatty Acid-amino Acid Conjugates Diversification in Lepidopteran Caterpillars

Fatty acid amino acid conjugates (FACs) have been found in noctuid as well as sphingid caterpillar oral secretions; in particular, volicitin [N-(17-hydroxylinolenoyl)-L-glutamine] and its biochemical precursor, N-linolenoyl-L-glutamine, are known elicitors of induced volatile emissions in corn plants. These induced volatiles, in turn, attract natural enemies of the caterpillars. In a previous study, we showed that N-linolenoyl-L-glutamine in larval Spodoptera litura plays an important role in nitrogen assimilation which might be an explanation for caterpillars synthesizing FACs despite an increased risk of attracting natural enemies. However, the presence of FACs in lepidopteran species outside these families of agricultural interest is not well known. We conducted FAC screening of 29 lepidopteran species, and found them in 19 of these species. Thus, FACs are commonly synthesized through a broad range of lepidopteran caterpillars. Since all FAC-containing species had N-linolenoyl-L-glutamine and/or N-linoleoyl-L-glutamine in common, and the evolutionarily earliest species among them had only these two FACs, these glutamine conjugates might be the evolutionarily older FACs. Furthermore, some species had glutamic acid conjugates, and some had hydroxylated FACs. Comparing the diversity of FACs with lepidopteran phylogeny indicates that glutamic acid conjugates can be synthesized by relatively primitive species, while hydroxylation of fatty acids is limited mostly to larger and more developed macrolepidopteran species.     

Ablation of Caterpillar Labial Salivary Glands: Technique for Determining the Role of Saliva in Insect–Plant Interactions

There has been an ardent interest in herbivore saliva due to its roles in inducing plant defenses and its impact on herbivore fitness. Two techniques are described that inhibit the secretion of labial saliva from the caterpillar, Helicoverpa zea, during feeding. The methods rely on cauterizing the caterpillar's spinneret, the principal secretory structure of the labial glands, or surgically removing the labial salivary gland. Both methods successfully inhibit secretion of saliva and the principal salivary enzyme glucose oxidase. Caterpillars with inhibited saliva production feed at similar rates as the untreated caterpillars, pupate, and emerge as adults. Glucose oxidase has been suggested to increase the caterpillar's survival through the suppression of inducible anti-herbivore defenses in plants. Tobacco (Nicotiana tabacum) leaves fed on by caterpillars with ablated salivary glands had significantly higher levels of nicotine, an inducible anti-herbivore defense compound of tobacco, than leaves fed upon by caterpillars with intact labial salivary glands. Tomato (Lycopersicon esculentum) leaves fed upon by caterpillars with suppressed salivary secretions showed greatly reduced evidence of hydrogen peroxide formation compared to leaves fed upon by intact caterpillars. These two methods are useful techniques for determining the role that saliva plays in manipulating plant anti-herbivore defenses.     

Does Aphid Infestation Interfere with Indirect Plant Defense against Lepidopteran Caterpillars in Wild Cabbage?

Attraction of parasitoids to plant volatiles induced by multiple herbivory depends on the specific combinations of attacking herbivore species, especially when their feeding modes activate different defense signalling pathways as has been reported for phloem feeding aphids and tissue feeding caterpillars. We studied the effects of pre-infestation with non-host aphids (Brevicoryne brassicae) for two different time periods on the ability of two parasitoid species to discriminate between volatiles emitted by plants infested by host caterpillars alone and those emitted by plants infested with host caterpillars plus aphids. Using plants originating from three chemically distinct wild cabbage (Brassica oleracea) populations, Diadegma semiclausum switched preference for dually infested plants to preference for plants infested with Plutella xylostella hosts alone when the duration of pre-aphid infestation doubled from 7 to 14 days. Microplitis mediator, a parasitoid of Mamestra brassicae caterpillars, preferred dually-infested plants irrespective of aphid-infestation duration. Separation of the volatile blends emitted by plants infested with hosts plus aphids or with hosts only was poor, based on multivariate statistics. However, emission rates of individual compounds were often reduced in plants infested with aphids plus hosts compared to those emitted by plants infested with hosts alone. This effect depended on host caterpillar species and plant population and was little affected by aphid infestation duration. Thus, the interactive effect of aphids and hosts on plant volatile production and parasitoid attraction can be dynamic and parasitoid specific. The characteristics of the multi-component volatile blends that determine parasitoid attraction are too complex to be deduced from simple correlative statistical analyses.     

Role of trail pheromone in foraging and processionary behavior of pine processionary caterpillars Thaumetopoea pityocampa

Although caterpillars of Thaumetopoea pityocampa may mark their pathways with silk, this study shows that the material is essential to neither the elicitation nor maintenance of trail-following or processionary behavior. Trail following is dependent upon a pheromone the caterpillars deposit by brushing the ventral surfaces of the tips of their abdomens against the substrate. Earlier instars are strongly bound to their trail system; in the laboratory, caterpillars followed circular trails continuously for as long as 12 hr before breaking away from them. The trail pheromone is long-lived and soluble in nonpolar solvents, but its volatilization or degradation allows the caterpillars to distinguish new from aged trails. In contrast to trail following, processionary behavior, the head-to-tail, single-file movement of the caterpillars is dependent on neither silk nor the trail pheromone. Stimuli associated with setae found on the tip of the abdomen of the precedent caterpillar serve to hold processions together, and such stimuli take priority over those associated with either the trail pheromone or silk. Although the caterpillars discern trail strength and choose stronger over weaker trails, the trail marking system of the processionary caterpillar appears less sophisticated than those of other, previously studied species of social caterpillars, and colonies are relatively inefficient in abandoning exhausted feeding sites in favor of new food finds. In laboratory studies, females were more likely to lead processions than males, and leaders, regardless of gender, expended more energy in locomotion than followers.     

Induction of volatile emissions in maize by different larval instars of Spodoptera littoralis

Maize plants under attack by caterpillars emit a specific blend of volatiles that is highly attractive to parasitic wasps. The release of these signals is induced by elicitors in the caterpillar regurgitant. Studies suggest that plants respond differently to different herbivore species and even to different herbivore stages, thus providing parasitoids and predators with specific signals. We tested if this is the case for different larval instars of the noctuid moth Spodoptera littoralis when they feed on maize plants. Cut maize plants were incubated in diluted regurgitant from second, third, or fifth instar caterpillars. There were no differences in total amount released after these treatments, but there were small differences in the release of the minor compounds phenethyl acetate and -humulene. Regurgitant of all three instars contained the elicitor volicitin. To test the effect of actual feeding by the larvae, potted plants were infested with caterpillars of one of the three instars, and volatiles were collected the following day. The intensity of the emissions was correlated with the number of larvae feeding on a plant, and with the amount of damage inflicted, but was independent of the instar that caused the damage. We also used artificial damage to mimic the manner of feeding of each instar to test the importance of physical aspects of damages for the odor emission. The emission was highly variable, but no differences were found among the different types of damage. In olfactometer tests, Microplitis rufiventris, a parasitoid that can only successfully parasitize second and early third instar S. littoralis, did not differentiate among the odors of maize plants attacked by different instar larvae. The odor analyses as well as the parasitoid's responses indicate that maize odors induced by S. littoralis provide parasitoids with poor information on the larval developmental stage. We discuss the results in the context of variability and lack of specificity in odorous plant signals.     

Aposematism in Archips cerasivoranus Not Linked to the Sequestration of Host-derived Cyanide

This study addressed the question of how caterpillars of Archips cerasivoranus feeding upon Prunus virginiana cope with the cyanogenic compounds of their food. Analysis by ion chromatography showed that young and aged leaves of P. virginiana consumed by the caterpillars during spring have hydrogen cyanide potentials (HCN-ps) of 2,473 +/- 130 ppm and 1,058 +/- 98 ppm, respectively. Although less than 3% of the cyanide released as the caterpillars feed escapes into the atmosphere, the larva's bright-yellow aposematic coloration and conspicuous activity can not be attributed to the sequestration of cyanide. Only six of 25 samples of the caterpillars' defensive regurgitants collected from 12 field colonies contained cyanide (17.6 +/- 6.54 ppm), less than 5% of the quantity previously reported to occur in the regurgitant of the tent caterpillar M. americanum. Only seven of 13 caterpillars assayed had detectable quantities of cyanide in their bodies (3.9 +/- 0.9 ppm). The fecal pellets that encase the cocoon contained no cyanide, nor did the frass that litters the leaf shelters. The small quantities of cyanide that occur in the caterpillar compared to the HCN-p of ingested plant material appear attributable to paced bouts of feeding and the maintenance of a highly alkaline foregut that inhibits cyanogenesis.     

Communal Foraging Behavior and Recruitment Communication in Gloveria sp.

The caterpillars of Gloveria sp. mark trails with a pheromone they deposit by dragging the ventral surface of the tip of the abdomen along branch pathways as they move between their communal nest and distance feeding sites. The threshold sensitivity of the caterpillar for an extract prepared from the secretory site was approximately 0.5 × 10^–3 caterpillar equivalents/cm of trail. Bioassays show that Gloveria follows neither authentic trails of Malacosoma americanum nor artificial trails prepared from 5-cholestane-3-one, a chemical previously reported to elicit trail following from other social caterpillars. Although our observations show that fed caterpillars mark heavily as they return to their nest, we found no evidence that individual caterpillars are able to recruit hungry nestmates to new food finds. In this species, recruitment to food occurs only after many caterpillars have reinforced a trail to a newly discovered food source. In contrast, hungry caterpillars of the confamilial species M. americanum, tested under identical conditions, responded strongly to the postprandial trails of individual caterpillars and rapidly abandoned depleted sites in favor of new food finds. We postulate that the difference in the efficiency with which these two species recruit nestmates to food evolved in response to differences in the spatial distribution of their food supplies.     

Differential Impact of Herbivores from Three Feeding Guilds on Systemic Secondary Metabolite Induction,Phytohormone Levels and Plant-Mediated Herbivore Interactions

Phytochemical defense responses of plants are often herbivore-specific and can be affected by a herbivore’s feeding mode. However, comprehensive studies documenting the impact of multiple herbivores from different feeding guilds on induced phytochemical responses in distal leaves and its consequences for plant-mediated herbivore interactions are limited and findings are inconsistent. We investigated how herbivory by leaf-chewing caterpillars, cell-content feeding spider mites and phloem-feeding aphids and whiteflies affect secondary metabolomes and phytohormone levels in youngest, non-damaged cotton leaves (distal leaves). Furthermore, bioassays with caterpillars were conducted to assess their performance on distal leaves of plants infested with different herbivores. Caterpillars, and to a lesser degree spider mites, led to a systemic induction of terpenoids with negative consequences for caterpillar performance in the bioassays. Both herbivores reduced levels of various nutrients and potentially antioxidative compounds. Caterpillar damage increased levels of jasmonoyl-L-isoleucine and abscisic acid (ABA), whereas spider mite infestation had no effect on phytohormone levels. Aphid and whitefly infestation did not systemically affect secondary metabolites. Aphids decreased salicylic acid levels while whitefly-infested plants contained increased ABA levels. Neither aphid nor whitefly infestation affected caterpillar performance. In general, feeding mode of a herbivore can affect systemically induced changes in phytochemistry and plant-mediated indirect interactions even though the two phloem-feeding herbivores triggered different phytohormonal responses. The observed reduction of nutrients and potentially antioxidative compounds upon caterpillar and spider mite herbivory underlines the importance of further elucidating the role of resource sequestration as a potential systemic defensive response following herbivory by chewers and cell-content feeding herbivores.     

Effects of Ingested Secondary Metabolites on the Immune Response of a Polyphagous Caterpillar <Emphasis Type="Italic">Grammia incorrupta</Emphasis>

We considered the effects of plant secondary metabolites on the immune response, a key physiological defense of herbivores against pathogens and parasitoids. We tested the effect of host plant species and ingested iridoid glycosides on the immune response of the grazing, polyphagous caterpillar, Grammia incorrupta (Arctiidae). Individuals of G. incorrupta were fed either one of three plant diets with varying secondary metabolites, or an artificial diet with high or low concentrations of iridoid glycosides. An immune challenge was presented, followed by measurement of the encapsulation response. We failed to detect a significant difference in the immune response of G. incorrupta feeding on diets with varying concentrations of iridoid glycosides, or feeding on different host plants. However, the immune response was lower in caterpillars consuming the artificial diet compared to those consuming the plant diets. When caterpillar performance was measured, pupal weights were lower when caterpillars ingested high concentrations of iridoid glycosides due to a decrease in feeding efficiency. Overall, individuals of G. incorrupta that consumed different plant diets exhibited a high immune response with low variation. We conclude that the immune response of G. incorrupta is adapted to feeding on a variety of plants, which may contribute to the maintenance of this caterpillar’s polyphagous habit.     

Predator Responses to Sequestered Plant Toxins in Buckeye Caterpillars: Are Tritrophic Interactions Locally Variable?

Recent studies demonstrate that generalist insect herbivores may be more subject to predation than specialists and suggest that this pattern is related to the availability and utilization of plant-derived natural products in diets of the latter. This intuitively attractive hypothesis has seldom been tested under natural conditions, however. A well-described plant-insect system, the buckeye butterfly, Junonia coenia, and its iridoid glycoside-containing host plants, was used to test the hypotheses: (1) that larval sequestration of iridoids reduces predation in the field, and (2) that this protection varies among populations. Fifth-instars reared in the laboratory on leaves of two host-plant species, Kickxia elatine (Scrophulariaceae) or Plantago lanceolata (Plantaginaceae), or on artificial diets were attached to monofilament tethers and set out into four natural populations. Only larvae fed on the locally available host plant and artificial diet-fed caterpillars were used at each site. Despite high overall predation, significantly more leaf-fed caterpillars survived than did artificial diet-fed caterpillars in Plantago sites, but the trend was not significant in Kickxia sites. The results reflect the differences in iridoid glycoside availability in these two host-plant species. They indicate that predators exert a strong selective force on this insect, that sequestered iridoid glycosides can be effective deterrents to predation, and that host-plant choices by ovipositing females and feeding larvae have consequences for mortality from natural enemies. This protection, however, is not absolute, and depends on local predator abundance and/or selectivity. The ecological interactions between buckeye caterpillars, their host plants, and their natural enemies are locally variable in nature.     

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.