Mixed blends of herbivore-induced plant volatiles and foraging success of carnivorous arthropods

Food webs are overlaid with infochemical webs that mediate direct and indirect interactions. Behavioural ecologists have extensively documented that carnivorous arthropods exploit herbivore-induced plant volatiles during foraging for herbivorous arthropods. Most studies on the role of infochemicals in multitrophic interactions have been conducted against an odour-free background, although field studies show that carnivores also use herbivore-induced plant volatiles under more complex conditions. Here we investigated the effect of mixing the blends of volatiles emitted by two plant species on the foraging behaviour of the predatory mite Phytoseiulus persimilis . This was done in an olfactometer under laboratory conditions and in a semi-field setup under greenhouse conditions. The olfactometer setup ensured directed mixing of the two odour blends, while odour mixing in the greenhouse setup was much less controlled and resulted from diffusion. In 4 out of 5 olfactometer experiments the behaviour towards volatiles from spider-mite ( Tetranychus urticae ) infested Lima bean plants was not affected by mixing with volatiles from caterpillar ( Pieris brassicae ) infested Brussels sprouts plants. In the fifth olfactometer experiment the response shifted significantly towards the volatiles from infested Lima bean leaves without volatiles from infested cabbage leaves. In the greenhouse setup no effect of infested cabbage plants or their volatiles on the location of spider-mite infested bean plants was recorded. The two odour blends used in this study, i.e. those from spider-mite infested Lima bean leaves and from caterpillar-infested Brussels sprouts plants, are very different and there is no overlap in compounds that are known to attract the predators. The results are discussed in the context of other types of odour-blend mixing and the effects on food web interactions.     

Attraction of Phytoseiulus persimilis (Acari: Phytoseiidae) towards volatiles from various Tetranychus urticae-infested plant species

Plants infested with the spider mite Tetranychus urticae Koch, may indirectly defend themselves by releasing volatiles that attract the predatory mite Phytoseiulus persimilis Athias-Henriot. Several plants from different plant families that varied in the level of spider mite acceptance were tested in an olfactometer. The predatory mites were significantly attracted to the spider mite-infested leaves of all test plant species. No differences in attractiveness of the infested plant leaves were found for predatory mites reared on spider mites on the different test plants or on lima bean. Thus, experience with the spider mite-induced plant volatiles did not affect the predatory mites. Jasmonic acid was applied to ginkgo leaves to induce a mimic of a spider mite-induced volatile blend, because the spider mites did not survive when incubated on ginkgo. The volatile blend induced in ginkgo by jasmonic acid was slightly attractive to predatory mites. Plants with a high degree of direct defence were thought to invest less in indirect defence than plants with a low degree of direct defence. However, plants that had a strong direct defence such as ginkgo and sweet pepper, did emit induced volatiles that attracted the predatory mite. This indicates that a combination of direct and indirect defence is to some extent compatible in plant species.     

State-dependent and odour-mediated anemotactic responses of the predatory mite Phytoseiulus persimilis in a wind tunnel

Anemotaxis in the predatory mite Phytoseiulus persimilis (both well-fed and starved), has previously been studied on a wire grid under slight turbulent airflow conditions yielding weak, yet distinct, gradients in wind speed and odour concentration (Sabelis and Van der Weel 1993). Such conditions might have critically influenced the outcome of the study. We repeated these experiments, under laminar airflow conditions on a flat surface in a wind tunnel, thereby avoiding variation in wind speed and odour concentration. Treatments for starved and well-fed mites were (1) still-air without herbivore-induced plant volatiles (HIPV) (well-fed mites only), (2) an HIPV-free air stream, and (3) an air stream with HIPV (originating from Lima bean plants infested by two-spotted spider mites, Tetranychus urticae). Well-fed mites oriented in random directions in still-air without HIPV. In an air stream, starved mites always oriented upwind, whether plant odours were present or not. Well-fed mites oriented downwind in an HIPV-free air stream, but in random directions in an air stream with HIPV. Only under the last treatment our results differed from those of Sabelis and Van der Weel (1993).     

Response of predatory mites with different rearing histories to volatiles of uninfested plants

The behavioural response of the predatory mite Phytoseiulus persimilis to volatiles from several host plants of its prey, spider mites in the genus Tetranychus, was investigated in a Y-tube olfactometer. A positive response to volatiles from tomato leaves and Lima bean leaves was recorded, whereas no response was observed to volatiles from cucumber leaves, or leaves of Solanum luteum and Solanum dulcamara.Different results were obtained for predators that differed in rearing history. Predators that were reared on spider mites (Tetranychus urticae) on Lima bean leaves did respond to volatiles from Lima bean leaves, while predators that had been reared on the same spider mite species but with cucumber as host plant did not respond to Lima bean leaf volatiles. This effect is compared with the effect of rearing history on the response of P. persimilis to volatile allelochemicals of prey-infested plant leaves.     

Absence of odour-mediated avoidance of heterospecific competitors by the predatory mite Phytoseiulus persimilis

Arthropods use odours associated with the presence of their food, enemies and competitors when searching for patches. Responses to these odours therefore determine the spatial distribution of animals, and are decisive for the occurrence and strength of interactions among species. Therefore, a logical first step in studying food web interactions is the analysis of behaviour of individuals that are searching for patches of food. We followed this approach when studying interactions in an artificial food web occurring on greenhouse cucumber in the Netherlands. In an earlier paper we found that one of the predators of the food web, the predatory mite Phytoseiulus persimilis Athias-Henriot, used to control spider mites, discriminates between odours from plants with spider mites, Tetranychus urticae Koch, and plants with spider mites plus conspecific predators. The odours used for discrimination are produced by adult prey in response to the presence of predators, and probably serve as an alarm pheromone to warn related spider mites. Other predator species may also trigger production of this alarm pheromone, which P. persimilis could use in turn to avoid plants with heterospecific predators. We therefore studied the response of the latter to odours from plants with spider mites and 3 other predator species, i.e. the generalist predatory bug Orius laevigatus (Fieber), the polyphagous thrips Frankliniella occidentalis and the spider-mite predator Neoseiulus californicus (McGregor). Both olfactometer and greenhouse release experiments yielded no evidence that P. persimilis avoids plants with any of the 3 heterospecific predators. This suggests that these predators do not elicit production of alarm pheromones in spider mites, and we argue that this is caused by a lack of coevolutionary history. The consequences of the lack of avoidance of heterospecific predators for interactions in food webs and biological control are discussed.     

Arrestment responses of the predatory mite, Phytoseiulus persimilis, to steep odour gradients of a kairomone

ABSTRACT. The response of the predatory mite, Phytoseiulus persimilis Athias-Henriot, to steep gradients of a volatile kairomone emitted by its prey, Tetranychus urticue Koch, was studied in a vertical air flow chamber. The orientation to wind direction was eliminated by using an olfactometer that had an air stream approaching the predator from below a gauze screen upon which the predator walked. The steep gradient of odour was obtained by putting a cylinder filled with prey-infested leaves vertically below the screen. Starved predators were arrested in the odour patch by walking more slowly and tortuously than well-fed predators. The latter mites did not show a significant ortho- or klinokinetic response to the presence of odour. Both well-fed and starved predators showed a chemotactic response to steep gradients at the border of the circular odour patch. Predators that happened to walk out of the patch, frequently turned back to it. This response is presumably based on idiothetic information about the predator's immediately previous walking directions, because it occurred in the odour-free zone after passing the steep gradient of prey odour. Right-about turns can help the predator to stay in static odour plumes with steep gradients at the borders. This type of plume is present only close to the odour source. Further away from the source the odour plume tends to move to and fro due to variation in wind direction. For the predator to keep track of these snaking plumes the right-about turns are unlikely to be of any value because the response is of short duration and because the response to a moving plume appeared to be inadequate; by moving the cylinder below the screen (and consequently the odour patch) it was found that the predator turned back even if the odour gradient was made to pass the predator in the same direction as that of the predator's movement.     

Induced defence in detached uninfested plant leaves: effects on behaviour of herbivores and their predators

Summary Induction of plant defence against herbivores may include the attraction by volatile infochemicals of natural enemies of the herbivore. The emitted volatiles that mediate this attraction may also affect the behaviour of the herbivore itself. In this paper we investigate the response of the herbivorous spider miteTetranychus urticae and the predatory mitePhytoseiulus persimilis towards volatiles whose production is induced in detached Lima bean leaves. Detached uninfested Lima bean leaves were incubated on wet cotton wool on which bean leaves infested with spider mites (T. urticae) were present simultaneously or had been present previously. These treatments induce the production of volatile infochemicals in the uninfested bean leaf tissue: predatory mites are attracted and spider mites are deterred. These are the first data on the response of predators and herbivores to plant volatiles whose production was induced in detached uninfested leaves.     

Evaluation of dry-adapted strains of the predatory mite Neoseiulus californicus for spider mite control on cucumber, strawberry and pepper

The goal of this study was to evaluate spider mite control efficacy of two dry-adapted strains of Neoseiulus californicus. Performance of these strains were compared to a commercial strain of Phytoseiulus persimilis on whole cucumber, pepper and strawberry plants infested with Tetranychus urticae at 50 +/- 5% RH. Under these dry conditions predators' performance was very different on each host plant. On cucumber, spider mite suppression was not attained by any of the three predators, plants 'burnt out' within 4 weeks of spider mite infestation. On strawberry, all predators satisfactorily suppressed spider mites yet they differed in short term efficacy and persistence. Phytoseiulus persimilis suppressed the spider mites more rapidly than did the BOKU and SI N. californicus strains. Both N. californicus strains persisted longer than did P. persimilis. The BOKU strain was superior to SI in population density reached, efficacy in spider mite suppression and persistence. On pepper, in the first 2 weeks of the experiment the BOKU strain was similar to P. persimilis and more efficacious in spider mite suppression than strain SI. Four weeks into the experiment the efficacy of P. persimilis dropped dramatically and was inferior to the SI and BOKU strains. Overall, mean predator density was highest on plants harbouring the BOKU strain, lowest on plants with P. persimilis and intermediate on plants with the SI strain. Implications for biocontrol of spider mites using phytoseiid species under dry conditions are discussed.     

Predation preferences and discrimination between con- and heterospecific prey by the phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus

Discrimination between and predation preference for con- or heterospecific larvae was examined for adult females of P. persimilis and N. californicus in plexiglass cages with and without their primary prey T. urticae. Rates of intra- and interspecific predation on larvae were measured for females held on leaves and provided with excess amounts of spider mites. Females of the generalist N. californicus distinguished con- and heterospecific larvae and preferred to prey upon the latter. Females of the specialist P. persimilis appeared to lack discrimination ability and fed equally on con- and heterospecifics. When spider mites and phytoseiids were offered simultaneously, all P. persimilis females chose to first attack T. urticae, whereas N. californicus females attacked both tetranychids and heterospecific phytoseiids. Females of both predators preyed upon phytoseiid larvae when held on leaves with surplus T. urticae: while P. persimilis fed on both con- and heterospecifics, N. californicus attacked larvae of P. persimilis but avoided cannibalizing larvae. The different behaviors of P. persimilis and N. californicus are discussed with regard to different predation types (generalists vs. specialists) and the possible consequences of mixed release for biological control of spider mites in greenhouses.     

Feeding History Affects the Response of the Predatory Mite Typhlodromus Kerkirae (Acari: Phytoseiidae) to Volatiles of Plants Infested with Spider Mites

The response of adult females of the predatory mite Typhlodromus kerkirae (Acari: Phytoseiidae) to volatiles emitted from bean leaves infested with Tetranychus urticae (Acari: Tetranychidae) or from leaves of Oxalis corniculata infested with Petrobia harti (Acari: Tetranychidae) was studied in the laboratory using a Y-tube olfactometer. Typhlodromus kerkirae females reared from larvae through to adults on T. urticae and pollen of Vicia faba responded to volatiles of bean leaves infested with T. urticae, either when they had a choice between infested and non-infested bean leaves or between bean leaves infested with T. urticae and O. corniculata leaves infested with P. harti. However, they did not respond when they had been reared only on the carotenoid-deficient pollen of V. faba. Female T. kerkirae that had been reared from larva to the tenth day of adult life on T. urticae and subsequently fed for 1 week on V. faba pollen did not respond to volatiles of bean leaves infested with T. urticae. In contrast, those that had been reared on V. faba pollen to the tenth day of adult life and subsequently fed for 1 week on T. urticae responded to volatiles of infested bean leaves.     

The Effects of Timing and Rates of Release of Phytoseiulus persimilis against Two-spotted Spider Mite Tetranychus urticae on Dwarf Hops

Single inoculative releases of the phytoseiid mite Phytoseiulus persimilis were made against the two-spotted spider mite, Tetranychus urticae, on two varieties of dwarf hops in 1996 and 1997 at means of 20, 10, 5, 2.5 and nil per plant, and at up to three timings. The numbers of spider mites recorded on leaves after the predators were released were related inversely to the rates of release. The earliest releases of the predator maintained spider mites at lower population densities than did those made later in the year. In all treatments the numbers of spider mites decreased when the prey:predator ratio reached approximately 10:1.     

Plants with spider-mite prey attract more predatory mites than clean plants under greenhouse conditions

Although many predators and parasitoids are known to respond to odours produced by plants infested with their prey under laboratory conditions, there are actually few studies that show that this response leads to higher numbers of predators or parasitoids on the plants under natural conditions. Here we study the response of predatory mites (Phytoseiulus persimilis Athias-Henriot, Acari, Phytoseiidae) to odours from cucumber plants infested with two-spotted spider mites (Tetranychus urticae Koch, Acari, Tetranychidae) in greenhouse release experiments, where predators were released in the centre of a hexagon of cucumber plants. Forty to 57% of all predators released were recaptured on plants within 7 h. Of these, an average of 79.5% were found on infested plants, indicating that these attract about 4 times as many predators as do clean plants. Hence, the blind predatory mites were guided to the plants with prey by herbivore-induced odours produced by the plant, as was indicated by olfactometer experiments, where it was found that P. persimilis preferred odours from infested cucumber plants to odours from clean cucumber plants. The long-range searching behaviour of P. persimilis is discussed.     

Hierarchical structure in kairomone preference of the predatory mite Amblyseius potentillae: dietary component indispensable for diapause induction affects prey location behaviour

ABSTRACT.

• 1 The phytoseiid predator Amblyseius potentillae (Garman) responded to volatile kairomones emitted from leaves infested by the two-spotted spider mite (Tetranychus urticae Koch), the apple rust mite (Aculus schlechtendali (Nalepa)) or the thrips Frankliniella pallida (Uzel), only when the predators had been reared on a carotenoid-free diet. In contrast A.potentillae responded to the European red spider mite (Panonychus ulmi (Koch)) both when the predators had been reared on a carotenoid-containing and a carotenoid-free diet.
• 2 Carotenoid-deficient predators did not respond to odour emitted from a host plant that was infested by larvae of the fruit-tree leaf roller (Adoxophyes orana (F.v.R)), a carotenoid-containing phytophage, that cannot be preyed upon by A.potentillae.
• 3 Carotenoids are indispensable for diapause induction in A.potentillae. Hence, carotenoid-deficient predators can increase their fitness by feeding from a carotenoid source. This may explain the response of carotenoid-deficient predators to the kairomones of the two-spotted spider mite, F.pallida and the apple rust mite (all containing ingestible carotenoids). As the fruit-tree leaf roller cannot serve as prey and thus as a carotenoid source, it makes sense that the predators lacking carotenoids do not respond to the kairomone of this phytophagous insect.
• 4 Two-choice experiments in a Y-tube olfactometer showed that the kairomone preference of A.potentillae has a hierarchical structure: the kairomone of the European red spider mite is the most preferred one, followed by that of apple rust mite, whereas the kairomone of the two-spotted spider mite is the least preferred of these three.

     

Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis

Jasmonic acid (JA) is a plant hormone that is involved in the induction of plant defence in response to herbivore attack. We studied the effect of exposure of gerbera leaves to JA on indirect plant defence, i.e. attraction of natural enemies of herbivores. Treatment of gerbera leaves with JA or feeding damage by the herbivorous spider mite Tetranychus urticae, both induced the production of a complex odour blend that attracts the predatory mite Phytoseiulus persimilis. This phytoseiid predator is a very effective biological control agent of the spider mite T. urticae. Comparison of headspace composition of gerbera leaves exposed to either JA or T. urticae revealed a large degree of resemblance, but some quantitative and qualitative differences were recorded. The major chemical group in both treatments is formed by the terpenoids which quantitatively comprised up to 80% of the total odour blend. These terpenoids included (E)-4,8-dimethyl-1,3,7-nonatriene, (E)--ocimene and linalool that are known to attract P. persimilis. Aldehydes, alcohols, esters and ketones, together with nitrogenous compounds formed the remaining constituents of the odour blend. The induction of predator attractants in plants by JA may be applied in biological control programs, which is discussed in this paper.     

Amblyseius andersoni Chant (Acari: Phytoseiidae), a successful predatory mite on Rosa spp

Roses on commercial nurseries commonly suffer from attacks by the two-spotted spider mite, Tetranychus urticae, which have a negative influence on growth and quality. The aim of this project is to find natural enemies that are well adapted to roses, and may improve biological control. At different sites such as a plant collection garden, public parks and field boundaries, leaves were sampled from roses to identify the indigenous species of predatory mites. Amblyseius andersoni was amongst other species frequently found, which suggests that this species thrives well on roses. The possibility for biological control of spider mites with A. andersoni was investigated both in container roses outdoors and in glasshouses. In plots of outdoor roses artificially infested with spider mites, the following treatments were carried out: spider mites alone (untreated plot), Amblyseius andersoni Amblyseius andersoni and ice plants, Neoseiulus californicus, Neoseiulus californicus and ice plants. There were four replications of the treatments. The ice plants, Delosperma cooperi, were added to some treatments to supply pollen as extra food for the predatory mites. Natural enemies such as Chrysoperla spp., Conwentzia sp., Orius sp., Stethorus punctillum, and Feltiella acarisuga occurred naturally and contributed to the control of spider mites. After one month the spider mites were eradicated in all treatments. At the end of the trial, predatory mites were collected from all plots for identification. The ratio of Amblyseius andersoni to Neoseiulus californicus was approximately 9:1. There was no obvious effect of the ice plants on the number of predatory mites. On a nursery, where new roses are bred and selected, Amblyseius andersoni was released in three glasshouses after one early treatment with bifenazate against two-spotted spider mite Tetranychus urticae. In two of these glasshouses Neoseiulus californicus was also released. Samples, which were taken in the summer months showed that the spider mites were kept at a very low level. Amblyseius andersoni was found, even if spider mites were absent. Rose plants infested with spider mites, that were brought in to the glasshouses later developed spider mite 'hotspots'. Phytoseiulus persimilis was introduced in the hot spots and contributed to the control along with Neoseiulus californicus, Amblyseius andersoni and naturally occurring Feltiella acarisuga. These observations showed that Amblyseius andersoni is a good candidate for preventing spider mite outbreaks, as it easily survives without spider mites. This predatory mite is able to survive on other food, including thrips and fungal spores.     

Evaluation of the predatory mite, Neoseiulus californicus, for spider mite control on greenhouse sweet pepper under hot arid field conditions

The efficacy of Neoseiulus californicus (a generalist predatory mite) for the biological control of Tetranychus urticae, was compared to release of Phytoseiulus persimilis (a specialist predatory mite) and an acaricide treatment in sweet pepper plants grown in greenhouse tunnels in a hot and arid climate. To ensure uniform pest populations, spider mites were spread on pepper plants in two seasons; a natural infestation occurred in one season. Predators were released prophylactically and curatively in separate tunnels when plants were artificially infested with spider mites, and at low and moderate spider mite populations when infestations occurred naturally. Although spider mite populations did not establish well the first year, fewer spider mites were recovered with release of N. californicus than with all other treatments. In the second year, spider mites established and the prophylactic release of N. californicus compared favorably with the acaricide-treated plants. In the course of monitoring arthropod populations, we observed a significant reduction in western flower thrips (Frankliniella occidentalis) populations in tunnels treated with N. californicus as compared with non-treated control tunnels. Our field trials validate results obtained from potted-plant experiments and confirm that N. californicus is a superior spider mite predator at high temperatures and low humidities.     

Lotus japonicus Infested with Herbivorous Mites Emits Volatile Compounds That Attract Predatory Mites

Lotus Japonicus has an indirect defense mechanism against spider mites, Tetranychus urticae, we investigated the responses of predatory mites, Phytoseiulus persimilis, to volatile compounds released from T. urticae-infested L. japonicus in a Y-tube olfactometer. Plants infested with spider mites attracted more P. persimilis than did clean air. Uninfested plants and artificially damaged plants did not attract P. persimilis. When infested by spider mites, L. japonicus plants started emitting (Z)-3-hexenyl acetate, (E)-4,8-dimethyl-1,3,7-nonatriene, germacrene d, 1-octen-3-ol and methyl salicylate (MeSA). These compounds were considered to be T. urticae-induced plant volatile compounds. When three L. japonicus mutants deficient in nodule organogenesis were infested by the spider mites, they all attracted P. persimilis. However, two of the infested mutants emitted blends of induced volatile compounds that were qualitatively different from those emitted from infested wild type L. japonicus. Received 8 August 2000/ Accepted in revised form 12 October 2000     

Evaluation of predatory mites and Acramite for control of twospotted spider mites in strawberries in north central Florida

Greenhouse and field experiments were conducted from 2003 to 2005 to determine the effectiveness of two predatory mite species, Phytoseiulus persimilis Athias-Henriot and Neoseiulus californicus (McGregor), and a reduced-risk miticide, Acramite 50 WP (bifenazate), for control of twospotted spider mite, Tetranychus urticae Koch, in strawberries (Fragaria x ananassa Duchesne). In greenhouse tests, three treatments consisting of releases of P. persimilis, N. californicus, and an untreated control were evaluated. Both species of predatory mites significantly reduced twospotted spider mite numbers below those found in the control during the first 3 wk of evaluation. However, during week 4, twospotted spider mite numbers on the plants treated with P. persimilis increased and did not differ significantly from the control. Field studies used releases of P. persimilis and N. californicus, applications of Acramite, and untreated control plots. Both N. californicus and P. persimilis significantly reduced populations of twospotted spider mite below numbers recorded in the control plots. During the 2003-2004 field season P. persimilis took longer than N. californicus to bring the twospotted spider mite population under control (< 10 mites per leaflet). Acramite was effective in reducing twospotted spider mite populations below 10 mites per leaflet during the 2003-2004 field season but not during the 2004-2005 field season, possibly because of a late application. These findings indicate that N. californicus releases and properly timed Acramite applications are promising options for twospotted spider mite control in strawberries for growers in north Florida and other areas of the southeast.     

Prey preference,intraguild predation and population dynamics of an arthropod food web on plants

The theory of intraguild predation (IGP) largely studies effects on equilibrium densities of predators and prey, while experiments mostly concern transient dynamics. We studied the effects of an intraguild (IG) predator, the bug Orius laevigatus, on the population dynamics of IG-prey, the predatory mite Phytoseiulus persimilis, and a shared prey, the phytophagous two-spotted spider mite Tetranychus urticae, as well as on the performance of cucumber plants in a greenhouse. The interaction of the predatory mite and the spider mite is highly unstable, and ends either by herbivores overexploiting the plant or predators exterminating the herbivores. We studied the effect of IGP on the transient dynamics of this system, and compared the dynamics with that predicted by a simple population-dynamical model with IGP added. Behavioural studies showed that the predatory bug and the predatory mite were both attracted to plants infested by spider mites and that the two predators did not avoid plants occupied by the other predator. Observations on foraging behaviour of the predatory bug showed that it attacks and kills large numbers of predatory mites and spider mites. The model predicts strong effects of predation and prey preference by the predatory bugs on the dynamics of predatory mites and spider mites. However, experiments in which the predatory bug was added to populations of predatory mites and spider mites had little or no effect on numbers of both mite species, and cucumber plant and fruit weight.