Odour-mediated responses of a predatory mirid bug and its prey, the two-spotted spider mite

It has been shown that many natural enemies of herbivorous arthropods use herbivore induced plant volatiles (HIPVs) to locate their prey. Herbivores can also exploit cues emitted by plants infested with heterospecifics or conspecifics. A study was conducted to test whether green bean HIPVs as well as odours emitted directly by spider mites influenced the orientation behaviour of the predatory mirid bug, Macrolophus caliginosus and its prey, Tetranychus urticae in a Y-tube olfactometer. Our results show that both spider mites and M. caliginosus preferred spider mite infested green bean plants to uninfested plants. For M. caliginosus this response was mediated by HIPVs whereas for T. urticae it was mediated through a composite response to both HIPVs and odours emitted directly by the conspecifics (and their associated products). The results may be of use in practical biocontrol situations, through e.g., plant breeding for improved HIPV production, conditioning of mass-reared predators to appropriate cues, and employment of “push–pull-strategies” by using HIPVs.     

Attraction of a generalist predator towards herbivore-infested plants

The occurrence and strength of interactions among natural enemies and herbivores depend on their foraging decisions, and several of these decisions are based on odours. To investigate interactions among arthropods in a greenhouse cropping system, we studied the behavioural response of the predatory bug Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) towards cucumber plants infested either with thrips (Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)) or with spider mites (Tetranychus urticae Koch (Acari: Tetranychidae)). In greenhouse release-recapture experiments, the predatory bug showed a significant preference for both thrips-infested plants and spider mite-infested plants over clean plants. Predatory bugs preferred plants infested with spider mites to plants with thrips. Experience with spider mites on cucumber leaves prior to their release in the greenhouse had no effect on the preference of the predatory bugs. However, this experience did increase the percentage of predators recaptured. Y-tube olfactometer experiments showed that O. laevigatus was more attracted to odours from plants infested with spider mites than to odours from clean plants. Thus, O. laevigatus is able to perceive odours and may use them to find plants with prey in more natural conditions. The consequences of the searching behaviour for pest control are discussed.     

Sub-lethal effects of fenbutatin oxide on prey location by the predatory mite <Emphasis Type="Italic">Iphiseiodes zuluagai</Emphasis> (Acari: Phytoseiidae)

We used a Y-tube olfactometer to assess the sub-lethal effects of the acaricide fenbutatin oxide on the olfactory response of the predatory mite Iphiseiodes zuluagai towards odours from: (1) air or undamaged coffee plants; (2) undamaged or red spider mite Oligonychus ilicis-infested coffee plants; (3) undamaged or false spider mite Brevipalpus phoenicis-infested coffee plants. Predatory mite adult females were exposed to residues of fenbutatin oxide or distilled water on leaf discs during a period of 72 h prior experiments. When exposed to distilled water (control treatments), predatory mites significantly preferred undamaged plants over air, O. ilicis-infested plants over undamaged plants, and they did not prefer B. phoenicis-infested plants over undamaged plants. However, predatory mites that had been exposed to residues of fenbutatin oxide were neither attracted towards undamaged plants nor to O. ilicis-infested plants. Thus, fenbutatin oxide affected negatively the olfactory response of I. zuluagai. We conclude that sub-lethal-effect studies should be considered in pesticide selectivity programs since the ability of predatory mites to locate their prey may be negatively affected by non-lethal concentrations of pesticides.     

Acaricides impair prey location in a predatory phytoseiid mite

The use of predatory mites as the sole management tactic in biological control programmes frequently does not fully and reliably prevents damage of phytophagous mites on plants. Therefore, as an alternative, the integration of predatory mites with acaricides can provide more effective control of phytophagous mites than that of the predators only. However, for such integration, acaricides minimal negative impacts on predatory mites are required. In this study, we evaluated the sublethal effects of three acaricides on the foraging behaviour of Neoseiulus baraki (Athias‐Henriot) (Acari: Phytoseiidae) in a coconut production system. The acaricides were assessed for interference with the location of prey habitat using a Y‐tube olfactometer and for interference with the location of the prey colony within the habitat using a video‐tracking system. In addition to the choice of odour source, the time required and the distance walked to make the choice were assessed. The acaricides tested were abamectin, azadirachtin and fenpyroximate. The predatory mite preferred coconuts infested with the coconut mite Aceria guerreronis Keifer (Acari: Eriophyidae) over uninfested coconuts when not exposed to acaricides. However, when exposed to acaricides, the predator did not distinguish between infested and uninfested fruits. When exposed to abamectin, N. baraki spent more time resting and walked greater distances before making the choice of an odour source. Thus, the acaricides impair the ability of the predatory mite N. baraki to locate a prey habitat and to locate a prey within that habitat. The acaricides differentially affected prey foraging by interfering with odour perception.     

Biological control of twospotted spider mite, <Emphasis Type="Italic">Tetranychus urticae</Emphasis>, with predatory mite, <Emphasis Type="Italic">Neoseiulus californicus</Emphasis>, in strawberries

Greenhouse and field experiments were conducted from 2005 to 2007 to determine the effectiveness of different release times with the predatory mite, Neoseiulus californicus (McGregor), for control of the twospotted spider mite (TSSM), Tetranychus urticae Koch, in strawberries (Fragaria x ananassa Duchesne). The effect of N. californicus releases over time and on development of TSSM populations during a growing season were evaluated. Our hypothesis was that repeated applications of N. californicus, which is currently recommended by biological control companies, might be unnecessary to attain season-long control of TSSM. In greenhouse trials, three treatments consisting of releases of N. californicus at five-day intervals: day 0, day 5, and day 10, and an untreated control were evaluated. The treatment releases significantly reduced TSSM below the control within five days of each release. Neoseiulus californicus significantly reduced TSSM in treatments with high densities (leaflets with ≥ 40 TSSM) below that of treatments with lower densities (leaflets with ≤ 10 TSSM) demonstrating that if released at a predator: prey ratio of 1:10, timing of release does not alter the effectiveness of N. californicus in controlling TSSM. However, we found that if the ratio of predator: prey remains adequate, N. californicus is a more efficient predator at high TSSM densities. Field studies included three treatments consisting of releases of N. californicus at one-month intervals. All treatments significantly reduced TSSM compared with the control plots (no releases). Releases applied early in the season sustained TSSM significantly below those in the control plots for the whole season. Our results indicate that one release of N. californicus is able to sustained control of TSSM in strawberry throughout a growing season if released when TSSM populations are low early in the season in the southeastern United States.     

Induced Response of Tomato Plants to Injury by Green and Red Strains of Tetranychus Urticae

We studied the induced response of tomato plants to the green strain and the red strain of the spider mite Tetranychus urticae. We focused on the olfactory response of the predatory mite Phytoseiulus persimilis to volatiles from T. urticae-infested tomato leaves in a Y-tube olfactometer. Tomato leaves attracted the predatory mites when slightly infested with the red strain, or moderately or heavily infested with the green strain. In contrast, neither leaves that were slightly infested with green-strain mites, nor leaves that were moderately or heavily infested with the red strain attracted the predators. We discuss the specific defensive responses of tomato plants to each of the two strains.     

How predatory mites find plants with whitefly prey

We investigated the searching behaviour of two species of predatory mites, Typhlodromips swirskii (Athias-Henriot) and Euseius scutalis (Athias-Henriot), both known to feed on immature stages of the whitefly Bemisia tabaci Gennadius. When released in a greenhouse inside a circle of cucumber plants that were alternatingly clean or infested with immature whiteflies, the mites took several days to find plants. Both species were recaptured significantly more on plants with whiteflies. This suggests that the mites are able to discriminate between plants with and without whiteflies. The predators may either have been attracted to plants with whiteflies from a distance or arrested on plants with whiteflies. Typhlodromips swirskii that had previously fed on whitefly immatures on cucumber leaves were significantly attracted by volatiles from cucumber plants with whiteflies in a Y-tube olfactometer. This suggests that the mites use volatile cues to discriminate between infested and clean plants. However, this response waned rapidly; if predators, experienced as above, were starved for 3–4 h in absence of cucumber leaves, they no longer preferred volatiles of infested plants to clean plants. Furthermore, T. swirskii that had no experience with immature whiteflies on cucumber plants also did not prefer odours of infested plants to those of clean plants. Because the release experiment with this species in the greenhouse was done with inexperienced predators, this suggests that the aggregation of mites on plants with whiteflies was mainly caused by differential arrestment of mites on plants with prey and clean plants. For T. swirskii, this was in agreement with the finding that the fraction of predators on plants with prey increased with time to levels higher than 70%. A less clear trend was found for E. scutalis, for which the fraction of predators on plants with prey stabilized soon after release to levels from 54–70%. Hence, the predatory mites may find plants with prey by random searching, but they are subsequently arrested on these plants. An earlier study showed that 87% of all whiteflies released in a set-up as used here were recaptured within 1 day. Hence, the effectiveness with which predatory mites locate plants with whiteflies is low compared with that of their prey. We expect this to generate spatial patterns in the dynamics of predator and prey and this may have consequences for biological control of whiteflies with predatory mites.     

Field predation of twospotted spider mite in a New Zealand strawberry crop

Predation by naturally occurring predatory arthropods was investigated to explain variations in population numbers of twospotted spider mite (Tetranychus urticae Koch) between first and second season strawberry crops. Araneomorph spiders. European harvestman [Phalangium opilio (L.)], Tasmanian lacewing [Micromus tasmaniae (Walker)] and Pacific damsel bug [Nabis kinbergii Reuter] were the only predators found in high numbers. However, spiders and harvestment were more prevalent than lacewings and nabids. Laboratory feedings trials indicated spiders build horizontal webs in the plants and prey predominantly on small flying insects that shelter in the crops. Similar feeding trials cofirmed the palatability of TSSM to spiders and harvestmen. Immunological testing for proteins of TSSM, aphids, Collembola and leafrollers in the intestines of field collected European harvestman, spiders, Tasmanian lacewing and Pacific damsel bug confirmed European harvestman includes TSSM in its diet, but not in large enough quantities to exert a significant regulating pressure on TSSM populations. Lacewings and nabids include TSSM in their diets but only in very small quantities (2% and 1% respectively). Spiders do not take TSSM unless they drop or spin down onto the spider webbing. The immunological testing also showed European harvestman to be a polyphagous and opportunistic feeder. Prey residues were detected more frequently in harvestmen intestines at times of prey abundance which indicated a seasonality to harvestmen diet.      

Factors affecting the distribution of a predatory mite on greenhouse sweet pepper

The predatory mite Neoseiulus cucumeris is used for biological control of phytophagous mites and thrips on greenhouse cucumber and sweet pepper. In a previous study, N. cucumeris provided effective control of broad mite but was only rarely found on the sampled leaves, raising questions about the factors affecting N. cucumeris distribution. To determine the distribution of N. cucumeris, leaves of pepper plants were sampled three times per day: just after sunrise, at noon and just before sunset for two years and throughout a 24 h period in one year. The presence of other mites and insects was recorded. Biotic (pollen) and abiotic (temperature, humidity) factors were monitored from the three plant levels. The effect of direct and indirect sunlight on the mites was assessed. N. cucumeris was found primarily in flowers; however, the mite’s distribution was affected by other predators (intraguild predation); in the presence of the predatory bug Orius laevigatus virtually no mites occurred in the flowers. Whereas temperature and humidity varied from the top to the lower level of the plants, apparently neither these factors nor the presence of pollen outside the flowers influenced mite distribution. N. cucumeris was found to be negatively phototropic; therefore N. cucumeris were pre-conditioned to light by rearing under light conditions for 4 months before being released. The light-reared mites were initially more numerous during the noon sampling period, however, rearing conditions caused only a temporary and non-significant change in distribution.     

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.     

Emission of volatile organic compounds by apple trees under spider mite attack and attraction of predatory mites

Emission rates of volatile organic compounds (VOCs) from Pirus malus L. subsp. mitis (Wallr.) var. Golden Delicious and var. Starking attacked by the phytophagous mite Panonychus ulmi Koch, and their attractiveness to the predatory mites Amblyseius andersoni Chant and Amblyseius californicus McGregor, were studied during three years. A large variability was found in the emission of individual VOCs depending on the infestation, the apple tree variety and the date. There were larger total VOC emission rates and larger total VOC leaf concentrations in apple trees attacked by phytophagous mites, especially in the var. Starking. In infested trees of this variety, there were also more predatory mites. An olfactometer assay showed that predatory mites preferentially chose branches infested by Panonychus ulmi (85% went to infested branches vs 15% to uninfested control branches) indicating that volatiles may be used as cues to find their prey.     

Introduction ofPhytoseiulus persimilis for twospotted spider mite control in greenhouses in Egypt [Acari: Phytoseiidae,tetranychidae]

The exotic predaceous mite,Phytoseiulus persimilis Athias-Henriot and the 2 native onesPhytoseius finitimus Ribaga andAmblyseius gossipi Elbadry were released on greenhouse cucumber plants in Egypt to examine their efficiency to control the twospotted spider miteTetranychus urticae Koch.P. persimilis proved to be sufficiently effective for the twospotted spider mite control under greenhouse conditions in Egypt. The 2 before-mentioned native predators were lost soon after release in the greenhouse although they are key mite predators on outdoor crops in this area.      

Variation in the olfactory response of 13 populations of the predatory mite Amblyseius womersleyi to Tetranychus urticae-infested plant volatiles (Acari: Phytoseiidae, Tetranychidae)

We studied the response of the predatory mite Amblyseius womersleyi collected in 13 different sites in Japan toward Tetranychus urticae-infested kidney bean leaf volatiles in a Y-tube olfactometer. The predatory mites were collected from eight plant species infested by one of three tetranychid mite species. The predators' responses to the infested-leaf volatiles varied from 33% to 97% among the populations. The predators collected at 10 sites showed a significant preference for infested-leaf volatiles, whereas those collected at three tea plantations did not distinguish between the infested- and uninfested-leaf volatiles. We discussed the possible factors that affected the olfactory response of A. womersleyi towards the infested leaf volatiles.     

Olfactory response of the predator <Emphasis Type="Italic">Zetzellia mali</Emphasis> to a prey patch occupied by a conspecific predator

While searching for food, predators may use volatiles associated with their prey, but also with their competitors for prey. This was tested for the case of Zetzellia mali (Ewing) (Acari: Stigmaeidae), an important predator of the hawthorn spider mite, Amphitetranychus viennensis (Zacher) (Acari: Tetranychidae), in black-cherry orchards in Baraghan, Iran. Using a Y-tube olfactometer, the response of this predatory mite was tested to odour from black-cherry leaves with a conspecific female predatory mite, either with or without a female of the hawthorn spider mite when the alternative odour came from black-cherry leaves with the hawthorn spider mite only. Female predators avoided odours from leaves with both a hawthorn spider mite and a conspecific predator, as well as leaves with a conspecific predator only. We discuss whether avoidance emerges in response to cues from the competitor/predator, the herbivore/prey or the herbivore-damaged plant.     

Control of the broad mite (Polyphagotarsonemus latus (Banks)) on organic greenhouse sweet peppers (Capsicum annuum L.) with the predatory mite, Neoseiulus cucumeris (Oudemans)

The predatory mite Neoseiulus cucumeris (Oudemans) (Acarina: Phytoseiidae) successfully controlled the broad mite Polyphagotarsonemus latus (Banks) (Acarina: Tarsonemidae) on two varieties of greenhouse-grown sweet peppers (Capsicum annuum L.). A survey of pre-plant seedlings showed that nurseries were a source of infestation for the broad mite. The predatory mites were released twice (on day 1 and 5, or 15 days later) on each plant, every second plant or every fourth plant. Broad mite populations were evaluated by sampling young leaves from the top of the plant. The effect of the broad mite on plant height, dry mass and yield was evaluated. Additionally, since N. cucumeris is known to control thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), blue sticky traps and flower sampling were used to evaluate changes in thrips populations. All three release rates of N. cucumeris significantly (P<0.05) controlled broad mite populations, but when the predatory mites were released only on every fourth plant, the overall height and yield of the plants were adversely affected by broad mites. Releasing N. cucumeris on each or every second plant was as efficacious in controlling broad mites as sulfur treatments in terms of plant height, dry mass and yield. Plants treated with sulfur, however, had significantly higher thrips populations and fruit damage.     

Olfactory response of predatory mites to vegetative and reproductive parts of coconut palm infested by <Emphasis Type="Italic">Aceria guerreronis</Emphasis>

The phytophagous mite Aceria guerreronis Keifer is an important pest of coconut worldwide. A promising method of control for this pest is the use of predatory mites. Neoseiulus baraki (Athias-Henriot) and Proctolaelaps bickleyi Bram are predatory mites found in association with A. guerreronis in the field. To understand how these predators respond to olfactory cues from A. guerreronis and its host plant, the foraging behavior of the predatory mites was investigated in a Y-tube olfactometer and on T-shaped arenas. The predators were subjected to choose in an olfactometer: (1) isolated parts (leaflet, spikelet or fruit) of infested coconut plant or clean air stream; (2) isolated parts of non-infested or infested coconut plant; and (3) two different plant parts previously shown to be attractive. Using T-shaped arenas the predators were offered all possible binary combinations of discs of coconut fruit epidermis infested with A. guerreronis, non-infested discs or coconut pollen. The results showed that both predators were preferred (the volatile cues from) the infested plant parts over clean air. When subjected to odours from different infested or non-infested plant parts, predators preferred the infested parts. Among the infested plant parts, the spikelets induced the greatest attraction to predators. On the arenas, both predators preferred discs of coconut fruits infested with A. guerreronis over every other alternative. The results show that both predators are able to locate A. guerreronis by olfactory stimuli. Foraging strategies and implications for biological control are discussed.     

Plant feeding by a predatory mite inhabiting cassava

Plant feeding by arthropod predators may strongly affect the dynamics of bi- and tri-trophic interactions. We tested whether a predatory mite, Typhlodromalus aripo, feeds upon its host plant, cassava. This predator species is an effective biological control agent of Monoychellus tanajoa (the cassava green mite or CGM) a herbivorous mite specific to cassava. We developed a technique to detect plant feeding, based on the use of a systemic insecticide. We found that T. aripo feeds upon plant-borne material, while other predatory mite species, Neoseiulus idaeus and Phytoseiulus persimilis, do not. Subsequently, we measured survival of juveniles and adult females of T. aripo and N. idaeus, both cassava-inhabiting predator species, on cassava leaf discs. Survival of T. aripo was higher than that of N. idaeus. Thus, T. aripo was able to withstand longer periods of prey scarcity. Because CGM populations fluctuate yearly and are heterogeneously distributed within plants, plant feeding may facilitate the persistence of populations of T. aripo in cassava fields and its control of CGM outbreaks. This revised version was published online in July 2006 with corrections to the Cover Date.     

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.     

Of mites and movement: the effects of plant connectedness and temperature on movement of Phytoseiulus persimilis

Simulation modelling studies on the biological control of Tetranychus urticae Koch in ornamental crops suggest that the dispersal of the predatory mite Phytoseiulus persimilis Athias-Henriot in the absence of food is important in determining its ability to locate sparsely distributed patches of prey (Skirvin et al., 2002). Experimental work to examine factors influencing dispersal of P. persimilis has shown that ground substrate affects the movement of the predator, and that the greater the number of connections between adjacent plants the greater the number of mites moving. In addition, P. persimilis are able to move across as many as 10 plant–plant connections within 24 h, although the majority of predators tracked moved less than this. Temperature has a significant impact on dispersal of P. persimilis, with more mites leaving release points as temperature increases up to 25 °C, but decreasing above this temperature. This work highlights the importance of understanding how the plant canopy and temperature influence the dispersal of predatory mites. The importance of these results for biological control in ornamental crops is discussed.     

Efficacy of carbon dioxide treatments for the control of the two-spotted spider mite, <Emphasis Type="Italic">Tetranychus urticae</Emphasis>, and treatment impact on plant seedlings

To develop a new control method for the two-spotted spider mite (TSSM), Tetranychus urticae, we investigated the effect of controlled atmospheres of carbon dioxide (CO₂) on TSSM mortality under different concentrations and treatment periods, and evaluated the impact of treatments on seedlings of five host plants of TSSM. Egg hatching rate of TSSM was reduced to 37.7, 5.4 or 0% after 24 h treatment involving concentrations of 16.7, 33.3 or 50%, respectively. Mobile stages (nymphs and adult) of TSSM were completely controlled after 24 h treatment at concentrations higher than 33.3%. After 4 h at concentrations of 33.3 or 50%, 1st-day survival rate for all mobile stages was 45.3 or 36.0%, respectively, whereas after 8 or 16 h treatments, all values were decreased to zero. Seedlings of four major host plants of TSSM (cucumber, eggplant, rape, green peppers) were damaged to varying degrees after 24 h at the three concentrations, but strawberry, another host plant, was not damaged. Cucumber suffered the most serious damage, resulting in wilting and death. In conclusion, controlled atmospheres of CO₂ can kill TSSM, particularly at high concentrations and with long treatment times. It can be used to control TSSM on strawberry, but should be used cautiously on other host plants.